Saline Soil - Based

Manoj Kumar · Hassan
Etesami Vivek Kumar

Editors
Saline Soil-
based
Agriculture
by
Halotolerant
Microorganisms
Saline Soil-based Agriculture by
Halotolerant Microorganisms
Manoj Kumar • Hassan
Etesami Vivek Kumar
Editors
Saline Soil-based
Agriculture by
Halotolerant
Microorganisms
Hassan Etesami
Editors Department of Soil Science
Manoj Kumar University of Tehran
Department of Life Sciences Tehran, Iran
Central University of Jharkhand
Ranchi, Jharkhand, India
Vivek Kumar
Himalayan School of Biosciences
Swami Rama Himalayan University,
Jolly Grant,
Dehradun, Uttarakhand, India
ISBN 978-981-13-8334-2 ISBN 978-981-13-8335-9 (eBook)

https://doi.org/10.1007/978-981-13-8335-9
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Preface
Food security is one of the fundamental needs that cannot be compromised by any
healthy society. The widespread increases in environmental damage and human
populations have an adverse effect on global food production, which may soon be
mixed with insufficient food before the global swelling population. To meet the
additional food demand, a significant increase (an estimated 50%) in yields of
major food crops is required for the projected population (around ten billion
people) by the next 50 years. The world’s population is constantly increasing,
while agricultural soils are constantly decreasing due to soil salinity. The costs
associated with this stress are potentially enormous (US$12 billion per annum
globally) and rising. Due to the decrease in the level of fertile land, saline soil-
based agriculture has been developing rapidly in recent years. A restriction to this
agricultural approach is low salt tolerance of agricultural crops and trees. In such
saline soils, the plants that are salt-resistant can produce significant yields. To
sustain future agricultural production in salt-affected soils, we must be able to
develop salt-tolerant food and fiber plants, which can successfully grow in salt-
affected areas. Developing salt-tolerant crops by traditional breeding and genetic
engineering has been a much desired scientific goal but with little success. An
alternative strategy to improve crop salt tolerance may be to introduce salt-tolerant
microbes that enhance crop growth. As soil salinity- resistant microorganisms
have increased the growth of many different crops grown in salt-affected soils, this
approach may succeed where it has proved difficult to develop salt-tolerant
germplasm. Identifying and making use of salinity-resistant microorganisms not
only meet our requirement of salt-tolerant crops but also reduce pressure on arable
lands. Salinity-tolerant microorganisms also offer excellent models for
understanding stress tolerance and mechanisms of adaptation and response that
can subsequently be engineered to crop plants to get over stress- induced climate
change. Recent advance in plant–bacteria interaction research revealed that plants
are able to shape their rhizosphere and endorhiza microbiome. Under stress
conditions, plants can require the presence of associated bacteria (stress tolerance)
for their growth and establishment in different ecosystems. Symbiotic bacteria
exist in all plants living in the natural ecosystems. This relationship may be the
key factor involved in plants’ stress tolerance ability. Indeed, local adaptation of
plants to their environment is driven by genetic differentiation in closely
associated bacteria.
v
vi Preface
Halophytes are extremely salt-tolerant plants which usually grow and survive
under salt concentrations as high as 5 g l—1, by maintaining negative water
potential, where no cultivation occurs. The salt-tolerant microbes inhabiting the
rhizosphere of halophytes may contribute to salt tolerance. The rhizosphere and
endorhiza of halophytic plants represent ideal source for isolation of various
groups of salt- tolerant microbes that could enhance the growth of different crops
under salinity stress. These salt-tolerant microbes are positive for multiple stress-
related traits that may facilitate plants to survive under growth inhibitory levels of
salt. The use of halotolerant microorganisms in agriculture as biofertilizers has
extremely increased as an alternative to replace agrochemicals. Halotolerant
microorganisms have begun to emerge as an important alternative to recuperate
abandoned farmland affected by salt in arid and semiarid areas. The
microorganisms isolated from halophytes were also able to increase the growth of
glycophytes (salt-sensitive crops) under salinity stress.
In this book, we offered a view of salt-tolerant microbes’ ability to increase
plant tolerance to salt to facilitate plant growth, the potential of halophytes’
rhizosphere as reservoir of beneficial salt-tolerant microbes, the future application
as bio-inoculants as alternative in agriculture, and a valuable resource for the
alternative way of improving crop tolerance to salinity and promoting saline soil-
based agriculture in the future. In general, this special collection of reviews will
highlight some of the recent progresses made in applied aspects of plant
(halophytes)-microbe interactions and its contribution toward eco-friendly
approach in agri-ecosystem (saline soil- based agriculture).
We hope you like reading this book.
Ranchi, India Manoj Kumar

Tehran, Iran Hassan Etesami
Dehradun, India Vivek Kumar
Contents
1 Soil Salinity as a Challenge for Sustainable Agriculture and

Bacterial-Mediated Alleviation of Salinity Stress in Crop Plants . . . 1
Hassan Etesami and Fatemeh Noori
2 Restoration of Plant Growth Under Saline Soil by Halotolerant
Plant Growth-Promoting Rhizobacteria (PGPR)......................................23
Leila Bensidhoum, Sylia Ait Bessai, and Elhafid Nabti
3 Halotolerant Rhizobacteria: A Promising Probiotic for Saline
Soil-Based Agriculture...................................................................................53
Ankita Alexander, Avinash Mishra, and Bhavanath Jha
4 Development of Salt Tolerance in Crops Employing
Halotolerant Plant Growth–Promoting Rhizobacteria
Associated with Halophytic Rhizosphere Soils........................................75
Ashok Panda and Asish Kumar Parida
5 Halotolerant Plant Growth-Promoting Fungi and Bacteria as
an Alternative Strategy for Improving Nutrient Availability
to Salinity-Stressed Crop Plants..............................................................103
Hassan Etesami and Hossein Ali Alikhani
6 Bacterial Endophytes from Halophytes: How Do They Help
Plants to Alleviate Salt Stress?...............................................................147
Ignacio D. Rodríguez-Llorente, Eloisa Pajuelo,
Salvadora Navarro-Torre, Jennifer Mesa-Marín,
and Miguel A. Caviedes
7 Effects of Halophilic Bacteria on Biochemical Characteristics
of Rice Cultivars Under Salinity Stress Conditions...............................161
Mehvish Riaz Khattak, Sami Ullah Jan, Ijaz Malook,
Sehrish Riaz Khattak, Nazneen Akhtar, Sehresh Khan,
and Muhammad Jamil
vii
viii Contents
8 Production of Rhamnolipids by a Halotolerant Bacterial

Strain with Seawater and Its Application in the Treatment
of Powdery Mildew of Strawberry (Fragaria ananassa)............................175
Xiangsheng Zhang and Boping Tang
9 Bottlenecks in Commercialization and Future Prospects of
Beneficial Halotolerant Microorganisms for Saline Soils.......................187
Bushra Tabassum, Adeyinka Olawale Samuel,
Muhammad Umar Bhatti, Neelam Fatima, Naila Shahid,
and Idrees Ahmad Nasir
10 Role of Halotolerant Microbes in Plant Growth Promotion
Under Salt Stress Conditions..................................................................209
Zahir Ahmad Zahir, Sajid Mahmood Nadeem,
Muhammad Yahya Khan, Rana Binyamin,
and Muhammad Rashid Waqas
About the Editors
Manoj Kumar is an Associate Professor at the Depart-

ment of Life Sciences, Central University of
Jharkhand, India. He is committed to high-quality
science that contributes to both improving our
understanding of plant development and increasing the
ecological niche. He has extensive professional
experience and has had affiliations with Jawaharlal
Nehru University and the Universities of Melbourne,
Pretoria, and Ton Duc Thang. His research focus
includes tree molecular genetics, plant-microbe
interaction, and bioremediation of soil pollutants.
He has authored 45 research papers and 5 review
articles in leading international journals as well as
13 books. He has also led several research projects and
R&D facilities at industry level and collaborated
internationally.
Hassan Etesami is a Research Scientist with 10 years

of experience in the field of soil biology and
biotechnology. He obtained his doctor’s degree from
the Depart- ment of Soil Science, College of
Agriculture & Natural Resources, University of
Tehran, Iran, where he is currently a Member of the
faculty. He has a special interest in developing
biofertilizers and biocontrol agents that meet farmers’
demands. He has coauthored over 50 publications
(research papers, review papers, and book chapters) in
various areas including biofertilizers and biocontrol.
He is also a Reviewer for 27 international journals.
ix
x About the Editors
His research areas include microbial ecology,

biofertilizers, soil pollution, integrated management of
abiotic (salinity, drought, heavy metals, and nutritional
imbalance) and biotic (fungal pathogens) stresses,
plant- microbe interactions, environmental
microbiology, and bioremediation.
Vivek Kumar is an Associate Professor, involved in

teaching and research and guidance. He works at
the Himalayan School of Biosciences, Swami Rama
Himalayan University, Jolly Grant, Dehradun, India.
He currently serves on the editorial boards of
numerous respected international journals. He is also a
Reviewer for several prestigious international journals.
In addition, he is an Evaluator of project proposals for
“The Netherlands Organisation for Scientific Research
(NWO),” Netherlands. He has published over 100
research papers, review articles, and book chapters and
has edited several Springer books. He also served as a
Microbiologist at the Department of Soil and Water
Research, Public Authority of Agricultural Affairs and
Fish Resources, Kuwait, for 8 years. He has been
credited with the first reporting and identification of
pink rot inflorescence disease of date palm in Kuwait
caused by Serratia marcescens. He was awarded
“Young Scientist Award” for the year 2002 in
“Agricul- tural Microbiology” by the Association of
Micro- biologists of India (AMI). His research areas
include plant-microbe interactions, sustainable
agriculture, environmental microbiology, and
bioremediation. He has also organized various
outreach activities.
Soil Salinity as a Challenge for Sustainable
Agriculture and Bacterial-Mediated 1
Alleviation of Salinity Stress in Crop Plants
Hassan Etesami and Fatemeh Noori
Abstract
Nowadays, the agricultural productivity is declining due to the negative effects of
climate change, global temperature rise, and increased environmental stresses.
Therefore, in order to achieve sustainable development in agriculture and to
increase agricultural products for feeding all of the world’s people, it seems
necessary to use the appropriate solutions and ecologically compatible and
environmentally friendly techniques to decrease the adverse effects of these
stresses on plant. Soil salinity is a problem for agricultural productivity around
the world. According to available reports, crops that grow in salt-affected soils
are subject to osmotic stress, poor physical soil conditions, nutritional disorders
and toxicity, and reduced crop yields. Limiting crop losses due to salinity stress
is a major area of concern to cope with the background of increasing food
requirements. Novel agricultural technologies are needed to improve food pro-
duction in salt-affected soils. Beneficial halotolerant rhizospheric bacteria
associated with plant have been known to increase plant tolerance to salinity
through mechanisms such as root system development, improved soil structure,
increased water and nutrient uptake, reduced sodium absorption, reduced nega-
tive effects of stress ethylene, and increased expression of genes involved in
resistance to salinity stress. Microbial inoculation to alleviate stresses in plants
could be a more cost-effective environment-friendly option which could be
H. Etesami (*)
Agriculture & Natural resources Campus, Faculty of Agricultural Engineering & Technology,
Department of Soil Science, University of Tehran, Tehran, Iran
e-mail: [email protected]
F. Noori
Department of Biotechnology and Plant Breeding, Sari Agricultural Sciences and Natural
Resources University, Sari, Iran
# Springer Nature Singapore Pte Ltd. 2019 1

M. Kumar et al. (eds.), Saline Soil-based Agriculture by Halotolerant
Microorganisms, https://doi.org/10.1007/978-981-13-8335-9_1
2 H. Etesami and F. Noori
available in a shorter time frame. Such inoculants contribute to the development

of sustainable agriculture under salinity-stressed conditions.
Keywords
Halotolerant PGPR · Salinity stresses · Agriculture crops · Plant · Microbe
interactions · Saline soil-based agriculture
1.1 Introduction
Food security is one of the basic needs of a human society that cannot be ignored
by any society. According to FAO (Food and Agriculture Organization), the total
demands for agricultural products will be 60% higher in 2030 than present time.
The world has depended on augmenting crop yields to supply an ever-enhancing
demand for food for over half a century (Ladha et al. 1998). Due to increasing
population growth, which is projected to reach 8.9 billion by 2050 according to
United Nations estimates (Wood 2001), and decreasing the fertility level of
agricultural soils, the ratio of acceptable agricultural land to population is
decreasing rapidly. Therefore, one of the main needs is to increase yield of crop
plants per unit area of land cultivation, especially in conditions of saline soils. The
soil with an electrical conductivity (EC) of the saturation extract (ECe) of 4 dS/m
(approximately 40 mM NaCl at 25 ○C) and exchangeable sodium of 15% is a
saline soil. The yield of most crop plants in such a soil is reduced, although many
crop plants showed yield reduction at lower ECes (Munns 2005). Different
definitions have been made for salinity. According to Shannon and Grieve (1998),
salinity is the excessive concentration of soluble salts and mineral elements in
water and soil solution that results in salt accumulation in the root zone, and the
plant encounters difficulty in absorbing sufficient water from the soil solution. In
another definition, salinity is excessive accumulation of soluble anions and cations
in a way that affects the growth of plants (Çavusoglu and Kabar 2010).
Soil salinization is a process in which the accumulation of soluble salts in the
surface layer of the soil increases, and as a result, the surface layer loses its
potential as the growth medium of the plants. In general, the soil salinization has a
primary or secondary origin. The primary origin of salinity is long-term natural
processes of accumulation of salts in the soil or in surface water. Secondary
salinity, which is also the result of human activity, is the result of irrigation, which
is widely responsible for increasing the concentration of dissolved salts in the soil
profile, which reduces plant growth and makes agricultural land unusable
(Egamberdieva et al. 2007; Manchanda and Garg 2008; Munns 2005). Irrigation of
agricultural land with saline water, inadequate irrigation management, recent
drought and low precipitation, high surface evaporation, and poor management
practices (poor cultural practices) are some of the main causes of increasing
salinity at a rate of 10% annually (Jamil et al. 2011). It is estimated that about 300
million hectares of land are irrigated in the world, of
1 Soil Salinity as a Challenge for Sustainable Agriculture and Bacterial... 3
which about 90% of the total water is spent generating 36% of global food
(Rengasamy 2006). In the regions that are not irrigated with irrigation water and
receive less rainfall and even in most agricultural land with higher temperatures,
there is a more increase in salinity levels (Othman et al. 2006). According to
forecasts, it has been determined that worldwide 33% of irrigated agricultural
lands and 20% of total cultivated are afflicted by high salinity. Climate change
may lead to even more saline landscapes in many nonirrigated regions (Othman et
al. 2006). It has been estimated that more than 50% of the arable agricultural land
would be salinized by the year 2050 (Jamil et al. 2011).
Among environmental stresses (i.e., extreme temperatures, high winds,
drought, soil salinity, and flood that have affected the production and cultivation
of agricultural crops), salinity stress is known as one of the most devastating
environmental stresses (i.e., low agricultural productivity, low economic returns,
and soil erosions) (Hu and Schmidhalter 2004) causing major reductions in
cultivated land area (Shahbaz and Ashraf 2013; Yamaguchi and Blumwald 2005)
and limiting the productivity and quality of crop plants (a 20–50% reduction in
plant yield), because most of the crop plants are sensitive to salinity due to high
concentrations of salts in the soil (excessive accumulation of nutrients in the form
of soluble salts) (Shrivastava and Kumar 2015). In addition to diminishing the
agricultural production of most crops especially salinity-sensitive crops, salinity
adversely affects soil physical and chemical properties and ecological balance of
the area (effect on the growth and diversity of organisms that live in or on soil
such as microbes, protozoa, and nematodes) (Hu and Schmidhalter 2004; Parida
and Das 2005). Due to the ever- increasing demand for food (production of 70%
more food crop for an additional 2.3 billion people by 2050 worldwide) and the
lack of salt-non-affected soils, we should inevitably use the potential of salinity-
stressed soils to produce important crop plants such as rice (Oryza sativa L.),
wheat (Triticum aestivum L.), and maize (Zea mays L.). It is predicted that a
significant increase (an estimated 50%) in grain yield of these plants is required to
fulfill the food supply requirements for the projected population by 2050 (Godfray
et al. 2010). As previously mentioned, salinity significantly reduces the growth
and yield of plants. In these areas, farmers are trying to compensate for losses
caused by salinity through the use of more inputs such as chemical fertilizers.
However, the use of chemical fertilizers, despite the high cost, low efficiency, and
the risk of environmental pollution such as surface water and groundwater
contamination, results in more soil salinization. Therefore, it is necessary to
better manage the saline soils in order to better utilize them. Many strategies have
been proposed to manage salinity soils (saline soil remediation) and increase plant
growth in these soils (Bai et al. 2017; Bauder et al. 2004; Etesami and Maheshwari
2018; Qadir et al. 2000; Tejada et al. 2006; Wang et al. 2014). Although the use of
strategies like leaching of salt from root zone, changed farm management
practices, the use of organic amendments, resource management practices, drip or
micro-jet irrigation to optimize use of water, shifting the crop calendars, the use of
salt-tolerant plants, and development of salinity-tolerant varieties through breeding
and genetic engineering to sustainable management can ameliorate yield reduction
under salinity stress, implementation is often limited due to cost and availability of
good water quality or water resource. In other words, such strategies are long
drawn and expensive processes (Araus et al. 2008; Dwivedi et al. 2010; Flowers
2004; Manchanda and Garg 2008; Shrivastava and Kumar 2015; Venkateswarlu
and Shanker 2009). Therefore, there is a need to develop low-cost and simple
biological methods for managing salt-affected soils, which can be used on short-
term basis. It is known that beneficial halotolerant microorganisms associated with
crop plants could play a significant role in this respect (Etesami 2018; Etesami and
Beattie 2017; Etesami and Maheshwari 2018; Shrivastava and Kumar 2015). In
this chapter, the effects of salinity stress on plants and the role of halotolerant
plant growth- promoting bacteria (PGPB) associated with plants in increasing the
plant’s resistance to salinity in saline soils are discussed.
1.2 Salinity Effect on Growth of Plants and Mechanisms

of Salinity Tolerance in Plants
Salinity as a major abiotic stress hampers crop productivity worldwide and limits
the increase in demand for food crops. More than 45 ha (about 20%) of the
cultivated land around the world is affected by salinity stress, and the amount is
enhancing day by day. Based on their adaptive evolution, some plant can
withstand salinity (halophytes), and some others cannot withstand salinity and
eventually die (glycophytes). Majority of major crop species that belong to
glycophytes (Flowers 2004; Munns and Tester ¼ 2008) are susceptible to salinity
stress (EC 3–5 dSm—1) (Horneck et al. 2007; Ondrasek et al. 2009), and their
productivity is considerably reduced due to improper nutrition of the plant
(Chinnusamy et al. 2005; Mantri et al. 2012).
Salinity stress affects almost all aspects of plant development (i.e., germination,
vegetative growth, and reproductive development) (Bano and Fatima 2009).
Depending on the severity and duration of stress, salinity stress results in changes
in various metabolic and physiological processes and morphological traits of
salinity-stressed crop plant such as diminished stomatal aperture (decrease in
stomatal conductance), interruption of membranes, decrease in the expansion of
the leaves, decrease in chlorophyll content and photosystem II efficiency,
disruption of photosynthetic functions through inhibition of nitrate reductase
(NR) activity, and premature aging of leaves (which affects process such as
photosynthesis and results in stunted growth); causes cell swelling and reducing of
energy production; adversely affects various enzymes activities (e.g., inhibition of
the activity of enzymes involved in nucleic acid metabolism); adversely affects
germination, plant vigor, crop yield, and the inhibition of root growth; impairs the
ability to detoxify reactive oxygen species (ROS) and accelerated defoliation and
senescence; adversely effects on all the major processes such as photosynthesis,
protein synthesis, energy and lipid metabolism, nutritional imbalance, the
inhibition of phytohormone synthesis and maturation of cell walls, hormonal
imbalance like elevated levels of ethylene (C2H4) (which at higher concentrations
imparts drastic effects on plant health, including defoliation and other unbalanced
cellular processes), differences in the antioxidant enzymes, physiological
disorders (like abscission, epinasty, senescence, and
susceptibility to diseases), and decrease in photosynthetic activity (Arbona et al.

2005; Barnawal et al. 2014; Cramer and Nowak 1992; Dantas et al. 2005;
Dolatabadian et al. 2011; Flowers 2004; Glick 2014; Hashem et al. 2015; Kang
et al. 2014a; Munns 2002; Munns and Tester 2008; Nadeem et al. 2014; Netondo
et al. 2004; Nunkaew et al. 2015; Parida and Das 2005; Paul and Lade 2014;
Prakash and Prathapasenan 1990; Rahnama et al. 2010; Shirokova et al. 2000;
Tavakkoli et al. 2011); and ultimately inhibits the production of the crop (James
et al. 2011; Rozema and Flowers 2008).
In general, effects of salinity on salinity-stressed crop plants are the results of
complex interactions among biochemical, physiological, and morphological pro-
cesses such as plant growth, seed germination, and water and nutrient absorption
(Akbarimoghaddam et al. 2011). Among them, seed germination (the stages of the
development of roots) and early seedling growth are the most salt-sensitive plant
growth stages, because the seedling root is in direct contact with soil and is
affected by salt stress (Bae et al. 2006; Rahman et al. 2000). Due to increased
osmotic pressure, higher saline concentrations could reduce the germination
percentage (Atak et al. 2006; Neamatollahi et al. 2009) in various crops such as
soybean (Essa 2002), wheat (Egamberdieva and Kucharova 2009), rice (Xu et al.
2011), maize (Khodarahmpour et al. 2012), and faba bean (Rabie and Almadini
2005).
Initially, salinity stress, which is also considered as hyperosmotic stress, in the
form of osmotic stress suppresses plant growth, so that in the early stages of
salinity stress, root water absorption capacity diminishes and osmotic stress causes
loss of water from the leaves, which increases the accumulation of salt in the
salinity- stressed plant (Munns 2005). In addition to creating water-deficit
conditions in early phase, salinity stress, due to having higher ionic concentration,
can also cause ionic toxicity in plants inducing leaf senescence and change the
basic texture of the soil causing decreased soil porosity and subsequently reducing
water uptake (a form of a physiological drought) (Munns and Tester 2008).
By creating a low osmotic potential of soil solution (osmotic stress), nutritional
imbalances (deficiency of nutrients of N, Ca, K, P, Fe, Zn), specific ion effects
(salt stress), oxidative stress, or a combination of these factors, salinity stress
causes many adverse effects on plant growth and development (Ashraf 2004; Bano
and Fatima 2009; Grover et al. 2011) at physiological and biochemical levels and
at the molecular level (Tester and Davenport 2003) resulting in substantial loss to
crop productivity.
Soil salinity significantly reduces uptake of plant nutrients such as P (due to
precipitation of phosphate ions with Ca ions) (Bano and Fatima 2009), N, K, and
Mg (Heidari and Jamshid 2010; James et al. 2011). Salinity also reduces
nitrogen
(N) incorporation to agricultural systems, which lead to a reduction in the
application of chemical N fertilizers, by adversely affecting leguminous plants,
which are sensitive to salinity. Only a few agronomical legumes can grow in
saline soils (Ashraf and McNeilly 2004). Soil salinity particularly disturbs the
symbiotic interaction between legumes and Rhizobium bacteria. Rhizobial
bacteria fix atmospheric nitrogen through the nitrogenase complex in root nodules
and make it available to the leguminous plants (Quispel 1988). For example,
salinity stress has decreased
nitrogen fixation by a failure of the infection and nodulation process and decrease
of activity of nitrogenase enzyme in several legumes such as Phaseolus vulgaris
(common bean), Glycine max (soybean), and Vicia faba (faba bean) (Rabie et al.
2005; Singleton and Bohlool 1984). Salinity reduces symbiotic legume growth by
diminishing the growth of roots, root tips, and root hairs, thereby decreasing sites
for potential rhizobial infection and further nodule development. Salinity-mediated
decrease of root growth has been attributed to reduced calcium absorption by the
plant in saline conditions (Bouhmouch et al. 2005).
For survival in saline soils, plants have to adapt and acclimatize to their
surrounding environment (Paul and Lade 2014). Plants develop different
physiological and biochemical mechanisms to survive in salt-affected soils.
Many mechanisms are known in plants through which plants increase their
resistance to salinity. The most important of these mechanisms are the
following: (i) hormone modulation,
(ii) biosynthesis of osmoprotectants and compatible solutes, (iii) ion compartmen-
talization and homeostasis, (iv) ion transport and uptake, (v) activation of antioxi-
dant enzyme and synthesis of antioxidant compounds, (vi) synthesis of
polyamines, and (vii) generation of nitric oxide (NO) (Gupta and Huang 2014). In
addition to these mechanisms, various studies have shown that microbial
(bacterial) communities associated with plant can also play a major role in
increasing plant growth and tolerance of plant to environmental stresses including
salinity stress in salt-affected soils (Etesami and Beattie 2018; Etesami and
Maheshwari 2018).
1.3 Bacterial-Mediated Alleviation of Salinity Stress in Crop

Plants
Plant-associated beneficial microorganisms including rhizoplane, rhizosphere and

endophytic bacteria, and mycorrhizal fungi can play an important role in
conferring plant resistance to salinity stress (Dodd and Pérez-Alfocea 2012;
Etesami and Beattie 2017, 2018; Etesami and Maheshwari 2018; Gill et al. 2016;
Hamilton et al. 2016; Singh et al. 2011; Vimal et al. 2016). PGPR (plant growth-
promoting rhizobacteria) colonize the rhizosphere of many plant species and
confer beneficial effects (Glick et al. 2007; Van Loon et al. 1998). Plants
inoculated with these bacteria induce biochemical and morphological
modifications leading to augmented tolerance to abiotic stresses including salinity
stress defined as IST (induced systemic tolerance) (Glick 2014; Kaushal and Wani
2016; Yang et al. 2009).
Compared to previous research, which had been focused on the
microorganisms that improve soil quality and fertility, current research is focused
mostly on microorganisms that can alleviate abiotic stress including soil salinity
(Mapelli et al. 2013). It is known that, by high osmotic strength and toxic
effects, salinity negatively affects activity of soil microorganisms including soil
bacteria. However, the bacteria inhabiting the sites exposed to frequent salinity
stress conditions or associated with halophytic plants are likely to be more
adaptive or tolerant and can survive and proliferate in the soil and in the
rhizosphere in a harsh environment (Etesami and Beattie 2018; Garcia and
Hernandez 1996; Paul et al. 2005). It has been
proven that salinity-tolerant bacteria may serve as better plant growth promoters
under salinity conditions (Etesami and Beattie 2018; Shrivastava and Kumar
2015). Among the bacteria whose habitats are the soil, rhizobacteria (root-
associated bacteria) are more tolerant to salinity stress because salinity stress is
higher in the area around the root (rhizosphere) because of depletion of water by
the plant root, leading to an increment in both osmolality and ionic strength
(Tripathi et al. 1998). These PGPR are salinity tolerant up to at least 3% NaCl
(Egamberdieva et al. 2011) and are able to survive in the rhizosphere of plants due
to their persistence and competitiveness under saline arid soil conditions (Mayak
et al. 2004b; Yasmin et al. 2007). The bacteria isolated from these areas also had
growth-promoting properties like indole-3-acetic acid (IAA) production,
phosphate solubilization, 1-aminocyclopropane-1-carboxylate (ACC) deaminase
activity, ammonia production, and nitrogen fixation (Etesami and Beattie 2018;
Mapelli et al. 2013). The halotolerant and halophilic microorganisms could
accumulate osmolytes in stress conditions (Zhou et al. 2015). Extensive research
has been conducted to show the beneficial effects of halotolerant PGPR on plant
growth (Table 1.1) (Etesami and Beattie 2017, 2018; Etesami and Maheshwari
2018). Salt-tolerant PGPR significantly increased the growth and yield of various
plants such as wheat (Barra et al. 2016; Egamberdieva and Kucharova 2009; Nabti
et al. 2010; Nia et al. 2012; Orhan 2016; Rajput et al. 2013; Ramadoss et al. 2013;
Upadhyay and Singh 2015; Upadhyay et al. 2012), cucumber (Egamberdieva et al.
2011; Kang et al. 2014a; Nadeem et al. 2016), sweet potato (Yasmin et al. 2007),
Ocimum basilicum (Heidari et al. 2011), tomato (Albacete et al. 2008; Essghaier et
al. 2014; Mayak et al. 2004a; Tank and Saraf 2010), pepper, canola, bean
(Egamberdieva 2011), lettuce (Barassi et al. 2006; Yildirim and Taylor 2005;
Yildirim et al. 2011), cotton (Yao et al. 2010), potato (Shaterian et al. 2005b),
Glycine max L. (Kang et al. 2014b; Naz et al. 2009), Oryza sativa L. (Jha et al.
2011), white clover (Han et al. 2014), Arachis hypogaea (Shukla et al. 2012),
strawberry (Esitken et al. 2010), Medicago truncatula (Bianco and Defez 2009),
groundnut (Saravanakumar and Samiyappan 2007), and Galega officinalis
(Egamberdieva et al. 2013) in salt-affected soil.
1.3.1 Mechanisms of Action by Which PGPR Alleviate Salt Stress
Halotolerant PGPR including Azospirillum, Rhizobium, Bacillus, Pseudomonas,

Pantoea, Paenibacillus, Enterobacter, Burkholderia, Achromobacter,
Microbacterium, Methylobacterium, Flavobacterium, Arthrobacter, Serratia,
Mycobacterium, Oceanobacillus sp., Halomonas sp., Exiguobacterium sp.,
Zhihengliuella, Variovorax, Microbacterium, Brachybacterium, Brevibacterium,
Haererohalobacter, Staphylococcus, Kocuria, etc. (Adesemoye et al. 2008;
Egamberdieva and Kucharova 2009; Egamberdieva et al. 2011; Egamberdiyeva
2007; Egamberdiyeva and Islam 2008; Etesami and Beattie 2018; Rajput et al.
2013; Shrivastava and Kumar 2013; Shukla et al. 2012; Siddikee et al. 2010) can
use various mechanisms to increase plant tolerance to salinity stress and stimulate
plant growth and development (Dimkpa et al. 2009; Etesami and Maheshwari
2018;
Table 1.1 Some PGPR that have caused induced systemic tolerance (IST) in plants under salinity
stress, with their mechanism of action
PGPR Mechanism(s) of action Crop plant References
Pseudomonas sp. Increase in IAA and protein Ocimum Heidari et al.
contents basilicum (2011)
Achromobacter ACC deaminase Tomato Zhang et al.
piechaudii (2008)
Azospirillum Increase in abscisic acid content Maize Cohen et al.
lipoferum (2009)
Achromobacter ACC deaminase Pepper and Mayak et al.
piechaudii tomato (2004b)
B. subtilis and Increase in total soluble sugars Wheat Upadhyay et al.
Arthrobacter sp. and proline content (2012)
P. pseudoalcaligenes Increase in osmoprotectant and Rice Jha et al. (2011)
and B. pumilus antioxidant enzymes
Azospirillum Increase in N concentration Wheat Nia et al. (2012)
Planococcus IAA, ACC deaminase, and Wheat Rajput et al.
rifietoensis phosphate solubilization (2013)
S. haemolyticus and Accumulated osmolytes Chickpea Essghaier et al.
B. subtilis (2014)
Bacillus subtilis Increase in chlorophyll content White Han et al. (2014)
and decrease in malondialdehyde clover
content
Pseudomonas Enhanced Fv/Fm and electron Pinus Rincón et al.
fluorescens transport rate halepensis (2008)
A. brasilense Increase in leaf water content Arabidopsis Cohen et al.
decrease in MDA content (2015)
P. aurantiaca IAA production Wheat Egamberdieva
and Kucharova
(2009)
Phyllobacterium Improved plant nitrogen status Arabidopsis Kechid et al.
brassicacearum (2013)
B. cepacia and Gibberellins production Cucumber Kang et al.
Acinetobacter (2014a)
calcoaceticus
Pseudomonas putida Gibberellins production Soybean Kang et al.
(2014b)
Bacillus subtilis Cytokines production Lettuce Arkhipova et al.
(2007)
P. trivialis ACC deaminase Galega Egamberdieva
officinalis and Jabborova
(2013)
P. fluorescens ACC deaminase Arachis Saravanakumar
hypogaea and Samiyappan
(2007)
Azospirillum ACC deaminase Wheat Zaki et al. (2004)
lipoferum
Azospirillum ACC deaminase Maize Hamdia et al.
brasilense (2004)
(continued)
Table 1.1 (continued)

PGPR Mechanism(s) of action Crop plant References
Enterobacter spp. Antioxidant activities Tomato Kim et al. (2014)
Azospirillum Increased proline Maize Kandowangko
et al. (2009)
Azospirillum Polyamine Rice Cassan et al.
brasilense (2009)
Bacillus spp. Higher uptake of K+ in plant as Gladiolus Damodaran et al.
compared to Na+ (2014)
V. paradoxus Enhanced nodulation and Chickpea Belimov et al.
increased nitrogen content (2009)
Glick 2014; Glick et al. 2007; Grover et al. 2011; Lugtenberg and Kamilova 2009;
Lugtenberg et al. 2013; Mayak et al. 2004b; Shrivastava and Kumar 2015; Yang
et al. 2009). These mechanisms include:
(i) The production of phytohormones such as auxin (i.e., IAA), cytokinin, and
gibberellins. It is known that phytohormones are involved in plant growth
development and in stress responses including salinity stress (Shaterian et
al. 2005a) and augment different cellular defense systems for the protection
of plants from stressful conditions (Shaterian et al. 2005b). Under high
salinity conditions, the production of hormones, auxins, gibberellins, and
zeatin in the roots and leaves of salinity-stressed plants decreases (Pérez-
Alfocea et al. 2010; Sakhabutdinova et al. 2003), and thereby the
germination percentage and plant growth and development also diminish
(Sakhabutdinova et al. 2003; Werner and Finkelstein 1995). In addition to
the decrease in production of hormones, salinity also reduces the supply of
hormones (i.e., cytokinin) from root to shoot (Naqvi and Ansari 1974). It
has been shown that salinity has no effect on the production of hormones
(i.e., auxin) of salt-tolerant PGPR (Albacete et al. 2008; Egamberdieva and
Kucharova 2009). For example, in a previous study, it was found that salt-
tolerant PGPR such as A. brasilense could produce IAA at a concentration
of 200 mM NaCl (Nabti et al. 2010). In another study, salt-tolerant PGPR
like S. plymuthica RR2-5-10, S. rhizophila e-p10, P. chlororaphis TSAU13,
and P. fluorescens SPB2145 were shown to produce IAA at 1.5% NaCl
(Egamberdieva 2011, 2012). Bacterial hormones result in increased root
growth, root length (modulation of root system architecture), root surface
area, and number of root tips, leading to enhanced uptake of nutrients
thereby improving plant growth under salinity stress conditions (Dodd et al.
2010; Egamberdieva and Kucharova 2009; Etesami and Alikhani 2016;
Etesami et al. 2015a, b; Etesami and Beattie 2017; Kurepin et al. 2015;
Postma and Lynch 2011). In other words, increased rooting system (a root
system with large surface area and increased number of root hairs)
constitutes a greater root surface area that enables the plant to get more
nutrients from the soil (Boiero et al. 2007; Egamberdieva and
Kucharova 2009; Mantelin and Touraine 2004). For example, IAA-

producing PGPR (i.e., P. aurantiaca TSAU22, P. extremorientalis
TSAU6, and
P. extremorientalis TSAU20) significantly augmented wheat root growth up
to 40% and shoot growth up to 52% at 100 mM NaCl compared to non-
inoculated wheat plants (Egamberdieva and Kucharova 2009). Plants in
response to salinity stress produce abscisic acid (ABA) causing stomatal
closure to diminish transpirational loss of water and mediate root branching
to augment water uptake in salinity-stressed plants hence inducing leaf
growth (Tardieu et al. 2010). It has been reported that some PGPR (i.e.,
Azospirillum lipoferum) can increase ABA content in stressed plant (Cohen
et al. 2009). In general, by producing phytohormones, PGPR strains can
modulate hormonal balance of plant hormones thus enhancing plant growth
under salinity stress conditions (Postma and Lynch 2011).
(ii) Ion homeostasis and increasing the availability of plant nutrients by produc-
tion of siderophores (increased iron nutrition), enhancing transformation and
acquisition of nitrogen (N), solubilization of inorganic phosphates, and solu-
bilization of K-bearing minerals (Bell et al. 2015; Etesami et al. 2017;
Etesami and Maheshwari 2018). It is known that high Na+ concentration
inhibits uptake of nutrients of K, P, and N which are essential elements for
growth and development (Etesami and Maheshwari 2018). In other words,
salinity creates nutritional imbalances due to disturbance in conserved
intracellular ionic milieu (Nadeem et al. 2009). Salinity-stressed plants can
protect themselves by restricting Na+ entry, retrieving Na+ from xylem
stream for recircu- lation to roots and expelling Na+ from roots during saline
stress (Chinnusamy et al. 2006). According to previous studies, many PGPR
could reduce the overaccumulation of Na+ in salinity-stressed plants and
maintain the ion homeostasis (higher N, P, and K uptake resulting in
increased K+/Na+ ratio in plant) under salinity stress conditions (Belimov et
al. 2009; Bharti et al. 2014; Damodaran et al. 2014; Etesami and
Maheshwari 2018; Kang et al. 2014b; Mayak et al. 2004b; Nadeem et al.
2009; Tewari and Arora 2014).
(iii) reduction in stress-induced ethylene production. Depending upon its
concentration, the ethylene is involved in the plant developmental cycle,
and it may be inhibitory (an inhibitor of plant root elongation) or
stimulatory (i.e., seed germination, root hair development, stem elongation,
fruit ripening, etc.) (Glick 2005; Penrose et al. 2001; Siddikee et al. 2011).
Under salinity stress conditions, excessive production of ethylene hormone
results in reduced root and shoot growth (Glick et al. 2007). ACC
deaminase-producing bacteria convert ACC (a prerequisite for ethylene
production) into α-ketobutyrate and ammonia (supply of nitrogen and
energy). Furthermore, by removing ACC, PGPR diminish the deleterious
effect of ethylene, ameliorating stress and promoting salinity-stressed plant
growth. In general, by decreasing stress ethylene, ACC deaminase-
containing PGPR increase the number of lateral roots, lateral root length,
and root dry weight of salinity-stressed plants (Shahzad et al. 2010). It was
reported a direct correlation between bacterial ACC deaminase activity and
root growth (Shaharoona et al. 2006). Bacterial ACC deaminase mediated
longer roots, in turn, take up relatively more water
from deep soil under salinity stress conditions, thus increasing the water use
efficiency (WUE) of salinity-stressed plants (Zahir et al. 2008). The enzyme
ACC deaminase is present in many PGPR (Glick 2010) including salt-
tolerant PGPR (Etesami and Beattie 2018). Many studies have shown that
PGPR could increase plant growth and resistance to salinity through the
production of this enzyme (Ahmed et al. 2004; Etesami and Beattie 2018;
Glick 2014; Hamdia et al. 2004; Mayak et al. 2004a, b; Nadeem et al. 2007,
2009, 2013; Paul and Sarma 2006; Penrose and Glick 2003; Saravanakumar
and Samiyappan 2007; Zaki et al. 2004).
(iv) Synthesis of compatible solutes, also known as compatible osmolytes, such
as proline, sugars, glycine betaine, polyols, and choline (Essghaier et al.
2014). Compatible osmolytes are a group of chemically diverse organic
compounds that are polar, uncharged, and soluble in nature and do not
interfere with the cellular metabolism even at high concentration (Ford
1984; Saxena et al. 2013). By accumulating compatible solutes to maintain
the cell turgidity within boundaries acceptable for normal cellular
physiology and osmotically adjust themselves, salinity-stressed plants may
protect themselves from salt stress (Evelin et al. 2009; Gill and Tuteja 2010;
Serraj and Sinclair 2002). Previous studies also reported that PGPR such as
Azospirillum,
P. pseudoalcaligenes, Burkholderia, Arthrobacter, and Bacillus could
alleviate salinity stress in various plants through increasing the
concentration of compatible solutes such as proline, glycine betaine-like
quaternary compounds, free amino acids, and soluble sugars in salinity-
stressed plants (Bano et al. 2013; Barka et al. 2006; Bharti et al. 2014;
Cassan et al. 2009; Damodaran et al. 2014; Jha et al. 2011; Kandowangko et
al. 2009; Paul and Nair 2008; Sarma and Saikia 2014; Shintu and Jayaram
2015; Sziderics et al. 2007; Vardharajula et al. 2011).
(v) Synthesis of antioxidant enzymes. Generation of reactive oxygen species
(ROS), as by-products of cellular metabolism, is generally low in various
plant organelles during normal growth conditions (Gill and Tuteja 2010). It
is known that low levels of ROS may act as signaling molecule thus
activating stress response and defense pathways (Pitzschke et al. 2006).
However, response of plants to salinity stress is the increase in generation
(overproduction) of ROS (i.e., hydroxyl radical, superoxide radical, singlet
oxygen, hydrogen peroxide, and superoxide) (Ahmad and Umar 2011;
Andersen et al. 2004; Apel and Hirt 2004; Chaves et al. 2002; Groß et al.
2013; Zhang et al. 2016), which results in oxidative damages in different
cellular components, like DNA, lipids (lipid peroxidation), and proteins
(disruption of membrane-bound proteins and inhibition of protein
synthesis), decreased membrane fluidity, and loss of enzymatic activities,
interrupting vital cellular functions of salinity-stressed plants and ultimately
cell death (Dietz et al. 2016; Gill and Tuteja 2010; Gupta and Huang 2014).
In other words, salinity stress causes a secondary stress that is called
oxidative stress, which is production of ROS above threshold levels leading
to imbalance in cell homeostasis (Gill and Tuteja 2010). Plants, which are
equipped with antioxidant defense system constituting enzymatic
components such as CAT
(catalase), GPX (glutathione peroxidase), SOD (superoxide dismutase),

APX (ascorbate peroxidase), monodehydroascorbate reductase (MDHAR),
and GR (glutathione reductase) and nonenzymatic components like
glutathione, cys- teine, tocopherols, and ascorbate, can eliminate or
neutralize ROS to cope with the oxidative stress by the antioxidant defense
system and protect themselves against detrimental effects of ROS (Miller et
al. 2010). Various studies have shown that there is a strong correlation
between tolerance to oxidative stress and increasing concentration of
antioxidant enzymes in plants (Asada 1999; Gupta et al. 2005; Sairam and
Srivastava 2002). By producing enzymes of antioxidants, some PGPR can
also degrade ROS. High activities of antioxidant enzymes are also linked
with oxidative stress tolerance (Štajner et al. 1997). There is substantial
evidence reported that PGPR could alleviate salinity-induced oxidative
stress (ROS formation) in various plants through manipulation of
antioxidant enzymes (Damodaran et al. 2014; Han and Lee 2005; Kim et al.
2014; Sandhya et al. 2010; Wang et al. 2012). It is noteworthy that the
mechanisms underlying behind variations found in the antioxidant enzyme
levels as affected by bacteria in plants imparting stress are not clear yet
(Kaushal and Wani 2016), which requires further research in the future.
(vi) Production of volatile compounds (Kaushal and Wani 2016). These
compounds affect the plant signaling pathways (Bhattacharyya et al. 2015).
(vii) Altering plant-water relationships and enhancing osmotic adjustment (Creus
et al. 2004).
(viii) Controlling various plant diseases (a broad-spectrum of root and foliar
pathogens) by antibiosis, competition for space and nutrients, and induction
of systemic resistance in plants (Compant et al. 2005; Singh et al. 2011).
1.4 Conclusions
The microbial communities inhabiting the rhizosphere of halophytic plants, also

known as the rhizosphere microbiome, and the microbial communities inhabiting
salt-affected soils can play an important role in conferring resistance to plants
against salinity stresses in a sustainable and environment-friendly manner thus
ensuring increased crop yield in salt- affected soils and opening a new advanced
technology for combating salinity. PGPR can also increase nutrient uptake from
salinity-affected soils, thus reducing the need for using chemical fertilizers in
saline soils. Such inoculants help the development of sustainable agriculture
(helpful in reducing the use of agrochemicals and in restoring soil health) under
salinity-stressed conditions. Despite many studies done in this area, the
understanding of cross talks between halotolerant rhizobacteria and plants that
mediate these responses is still one major hindrance. In addition, the application of
halotolerant rhizobacteria as a bio-fertilizer requires more research in field
conditions.
Acknowledgment We wish to thank the University of Tehran for providing the necessary
facilities and funds for this study.
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Restoration of Plant Growth Under Saline
Soil by Halotolerant Plant Growth- 2
Promoting Rhizobacteria (PGPR)
Leila Bensidhoum, Sylia Ait Bessai, and Elhafid Nabti
Abstract
Saline soils are among the big obstacles in agricultural activities in arid and
semiarid regions. Numerous cultivated areas in the world’s irrigated soils are
severely affected by both of salinity and salinization. Therefore, the
development and sustainability of profitable agricultural systems are seriously
threatened. Sustainable and cost-effective plant growth becomes even more
important due to the need of energy-efficient plant growth for biomass and
bioenergy production, especially in soils of lower quality, in addition to food
production.
The utilization of halotolerant PGPRs (plant growth-promoting
rhizobacteria) could help plant growth to adapt to increased salinity by the
potential osmoregu- latory mechanism implicated in the cell function
regulation. Consequently, PGPRs provide plants with their activities to
challenge osmotic stress by supporting them in the restoration of essential
activities. These bacteria stimulate plant growth under saline conditions by
diverse mechanisms such as phytohormone production and ACC deaminase
synthesis to decrease inhibitory effect of ethylene occurring in plants under salt
stress conditions. Halotolerant PGPRs can also use the natural osmoprotectants
realized from marine algae to challenge salt stress. It is important to highlight
that halotolerant PGPRs stimulate plant growth under elevated salinity by using
similar mechanisms like other halosensitive bacteria.
Keywords
Halotolerant rhizobacteria · Plant growth · Salts stress · Inoculation · Restoration
L. Bensidhoum · S. Ait Bessai · E. Nabti (*)

Laboratoire de Maitrise des Energies Renouvelables, Faculté des Sciences de la Nature et de la
Vie, Université de Bejaia, Bejaia, Algeria
FSNV, University de Bejaia, Bejaia, Algeria
e-mail: nabtielhafi[email protected]

24 L. Bensidhoum et al.
2.1 Introduction
The rapidly increasing human population is causing a number of challenges to

sustain life on earth (Ashraf et al. 2012). In 2004, the United Nations estimated
that at the end of 2025 the human population will cross 8 billion (6.8 billion will
be in Asia and Africa), while at the end of 2050 it could be over 10 billion.
Therefore, to satisfy the nutrient demands of this growing population, the global
food production will need to increase by 38% by 2025 and by 57% by 2050 if
food supply to the growing world population is to be maintained at current levels
(Wild 2003).
This growing population requires increasing food quantity and quality,
especially in countries where resources are damaged due to uncontrolled human
activities and environmental degradation. Agriculture is the main source of food
for humans, and vegetables play an important role in humans’ diet by providing
and assisting the body with a variety of important constituents such as minerals,
vitamins, complex carbohydrate, high dietary fiber, low levels of fat, and high
amount of water. Agricultural production needs to jump by 70–100% to satisfy
global increased demands in the next few years (Lafe 2013). However, agriculture
practices are threatened by various biotic and abiotic stresses, which cause large
losses in crop production (Singh et al. 2014).
It is well known that the crop losses due to abiotic stresses are more severe than
those caused by the biotic ones (Ashraf et al. 2012). Nearly 82% of potential yield of
crops is lost due to abiotic stresses every year, and the available productive areas of
arable land are decreasing worldwide (Mona et al. 2016). The agricultural lands are
threatened by various environmental stresses such as salinity, drought, extreme
temperatures, pH, mineral deficiencies or toxicities, heavy metals, nutrient depletion,
soil erosion, etc. that seriously reduce plant yields (Chedlly et al. 2008; Anonymous
2015).
Among these constraints, the salinization of agricultural lands imposes
enormous challenges, both for scientists and for farmers, demanding a growing
exploitation of natural resources in search of promising solutions (Ashraf et al.
2012).
To alleviate salt stress in crop plant, several strategies have been applied; these
approaches include chemical amendment, improved irrigation practices, plant
breeding techniques, and plant genetic modification which are time-consuming,
difficult, and costly (Saghafi et al. 2013; Selvakumar et al. 2014; Shrivastava and
Kumar 2015). Using biological product, particularly plant growth-promoting
rhizobacteria (PGPRs), may prove to be a beneficial, cost-effective, and eco-
friendly strategy that can improve crop productivity and soil health under normal
and stressed environment. It presents a great scientific and agronomic interest
since they play an important role in biological functioning of the rhizosphere and
therefore improve growth, yield, and health of agricultural crops.
PGPRs, mainly bacteria belonging to the genera Arthrobacter, Azotobacter,
Azospirillum, Bacillus, Enterobacter, Pseudomonas, Serratia (Gray and Smith
2005), and Streptomyces spp. (Tokala et al. 2002), influence positively plant
health by improving its growth and/or protecting it against abiotic and biotic
stress. These microorganisms are able to grow and compete with other
microorganisms to occupy rhizosphere zone. Plant growth-promoting
rhizobacteria colonize the rhizosphere
2 Restoration of Plant Growth Under Saline Soil by Halotolerant Plant Growth... 25
using root exudates as nutrient substrates but unlike other rhizosphere bacteria
improve plant growth and health via a variety of mechanisms (Vacheron et al.
2013). Recent focus of research involves the use of PGPRs to alleviate salt stress
in plant. Kasim et al. (2016) showed that the deleterious effect of salt stress on
some plant growth parameters (seedling length, fresh and dry masses, as well as
relative
water content) was alleviated by bacterial inoculation.
2.2 Salinity and Salinization
Salinity is the second major limiting factor after drought, which is putting down
crop production and adversely impacts plant growth and crop production
worldwide, mainly in arid and semiarid regions (Pessarakli 1991; Saranga et al.
2001; Yadav et al. 2011).
Soil salinization is a term used for the accumulation of soluble salts in soils at a
level that negatively affects agricultural productivity, environmental health, and
economic welfare (Rengasamy 2006) that results in the formation of a salt-
affected soil (Ciseau 2006). It costs the world 12 billion US$ a year in reduced
income (Ghassemi et al. 1995).
In 2005, the FAO has estimated that over 6% of the total continent area equal to
an area of about 800 million hectares is salt affected in the world, by either
sodicity (434 million h) or salinity (397 million h). When there is a high
concentration of Na+ (sodium) in soil, it is referred to as “sodicity,” and when Cl—
(chloride) or other salts are involved, it is referred as “salinity.” It has been
estimated that worldwide 20% of total cultivated and 33% of irrigated agricultural
lands are afflicted by high salinity (Shrivastava and Kumar 2015).
2.2.1 Salinity
Salinity is considered as one of the most brutal environmental factors limiting the
crop plant productivity because most of the crop plants are sensitive to high
concentrations of salts in soil, and the area of land affected by it is increasing day
by day (Shrivastava and Kumar 2015). Of the global threats that collectively
compromise about 10 ha arable land per minute (Griggs et al. 2013), salinization
contributes about 30% (Buringh 1978), and due to this problem, the area that can
be used for agriculture is reducing by 1–2% every year, hitting hardest in arid and
semiarid regions (FAO 2002; Shilpi et al. 2008). It has been expected that 30% of
arable land is likely to become saline by 2025 (Munns 2002) and more than 50%
of all agricultural soils will be affected by salinity increase by 2050 (Jamil et al.
2011; Dikilitas and Karakas 2012; Stanković et al. 2015).
This alarming increase of salt-affected areas is due to various reasons such as
low precipitation, high surface evaporation (reduction of soil water content by
removing pure water as vapor), weathering of native rocks, irrigation with saline
water, exaggerated use of fertilizers, low rainfall, high temperature, and over-
irrigation
causing capillary movement of hidden salts from lower layers in soil and other
poor cultural practices (Yao et al. 2010; Shrivastava and Kumar 2015). According
to Patel et al. (2011), this continuing increase in salt-affected areas is due to the
introduction of irrigation in new areas, especially in arid and semiarid regions,
because such environment received less rainfall and then more water is transpired
to air and ultimately net water movement is upward leaving salts on soil surface.
2.2.2 Salinization
Soil salinization consists of water-soluble salt accumulation in soil that includes

cations such as sodium (Na+), potassium (K+), calcium (Ca2+), and magnesium
(mg2+) along with anions chloride (Clˉ), sulfate (SO42ˉ), nitrate (NO3ˉ), bicarbonate
(HCO3ˉ), and carbonate (CO32ˉ) (Diby and Harshad 2014).
Salts occur as ions, which may be released from weathering minerals in soil,
may be applied through irrigation water or as fertilizers, or sometimes migrate
upward in soil from shallow groundwater. When precipitation is insufficient to
leach ions from the soil profile, salts accumulate in soil resulting in a high salinity
(Blaylock 1994). Soil salinity in agriculture refers to high concentration of
soluble salts in soil moisture of the root zone (Diby and Harshad 2014).
According to Ghassemi et al. (1995), soil salinization may be either a natural
process, also known as primary salinization, or a human-induced
(anthropogenic) process, known as secondary
salinization.
The major causes of naturally induced salinity are intrusion of highly salinized
water in coastal (oceans and sea) or continental (fossil salt aquifers) regions,
aeolian by wind-borne salt from salt surface waters (oceans, lakes) deposited
inland, and dissolution of parent rock material. In contrast, secondary salinization
is mainly caused by some agricultural practices (irrigation with brackish water,
fertigation, application of inorganic/organic soil amendments, and improper
cropping patterns and rotations), deforestation, construction of reservoirs, salt
farming, etc. (Mitsuchi et al. 1986; Rengasamy 2006; Biggs et al. 2010).
In 2006, Rengasamy, based on soil and groundwater problem all over the
world, classified the salinity into three major types, differently to the classification
of “primary” or “secondary” salinity as defined by Ghassemi et al. (1995).
According to this classification, salinity may be associated to three sources:
(i) Groundwater-associated salinity (GAS), when water exits from ground to the
soil surface with upward movement, it brings dissolved salts in it, and at soil
surface, water will evaporate, and salts will be accumulated. It was reported
by Talsma (1963) that salt accumulation is high when the water table is less
than
1.5 m below the soil surface.
(ii) Non-groundwater-associated salinity (NAS), in this case, salts are introduced
by rain, weathering, and aeolian deposits and stored within the soil solum.
(iii) Irrigation-associated salinity (IAS), because of insufficient leaching, salts
introduced by irrigation water are stored within root zone.
Additionally, about one-third of the world’s irrigated lands contributing with

more than 30% of global agricultural production are salt affected (Munns and
Tester 2008), because irrigation modifies soil hydration balance by generating an
extra supply of water; this supply is always associated with added salts and
consequently results in soil becoming salty and unproductive (Wu et al. 2008).
Soil salinity is measured by passing an electrical current through a soil solution
extracted from soil sample, and the ability of this “saturated solution” to carry
current is called electrical conductivity (EC) (Shin et al. 2016).
In general, soils are considered to be saline if they have concentration sufficient
to interfere with the growth of most of crop species (Bui 2013); however, US
Depart- ment of Agriculture (USDA) (1954) defines a saline soil as one in which
EC measured in units of decisiemens/meter or millisiemens/cm of the saturation
extract (ECe) in the root zone exceeds 4 dS m—1 (approximately 40 mM NaCl) at
25○ and an exchangeable sodium percentage (ESP) of 15 or more.
2.3 Effects of Salinity on Soil, Plants, and Microorganisms
2.3.1 Effect on Soil Quality
Soil salinity is not a recent issue; it has been a major concern to global agriculture
throughout human history. It is considered as a major factor reducing crop produc-
tivity and a main cause to abandon lands designed for agricultural purposes (Dodd
and Perez-Alfocea 2012).
In addition, salinity not only decreases agricultural production of most crops
but also affects soil physicochemical as well as biological properties (soil quality)
and ecological balance of area (Benlloch-Gonzalez et al. 2005; Shrivastava and
Kumar 2015; Arshadullah et al. 2017); it is also responsible for low economic
returns (Hu and Schmidhalter 2002).
It is well documented that excess accumulation of salt leads to negative effects
on soil structure, increase in osmotic pressure, and decrease in water potential and
declines turgor potential of cells (plants and microbes). The most soil processes
that have immediate consequences for soil biological activity or soil conservation
occur within the soil pores (either in the pore space or on the surface of particles
forming the pores); for this reason, pores are considered as central physical
features in soil structure (Kay 1990; Rengasamy and Olsson 1991). However, the
elevation of sodium (Na+) concentration causes soil dispersion, swelling of the
clay platelets, and disruption of the forces involved in binding of clay particles.
These changes cause clay particles to plug soil pores (especially in fine-textured
soil horizons) (Burrow et al. 2002) leading to reduction in soil aeration
(prevalence of anaerobic conditions), water infiltration (deteriorating soil
hydraulic properties), and also soil compaction (Abu-Sharar et al. 1987). Thus,
excessive sodium concentration raises soil pH, soil erosion, and water runoff
(Ondrasek et al. 2010; Diby and Harshad 2014). Thereby, the presence of
multivalent cations can increase the sorption of organic matter to soil particles
(Mikutta et al. 2007; Mavi et al. 2012) and thus
reduces organic matter amount available for decomposition (Oades 1988; Six et al.
2000). Because of these modifications, soil becomes unsuitable for proper root
growth and plant development.
2.3.2 Effect on Plant Growth Activities
Salinity constitutes a most critical constraint, which hinders and causes a

significant decrease in agricultural production in many areas worldwide (Tank and
Saraf 2010). It is a limiting growth factor for many types of plants, especially non-
halophytic ones (Saghafi et al. 2013). Most of the widely used crops in human or
animal nutrition such as cereals, forages, or horticultural crops are susceptible to
excessive salt concentration either dissolved in irrigation water or already present
naturally in rhizosphere soil (Ondrasek et al. 2010). It was reported that vegetables
are more sensitive to salt than forages and grains (Waller and Yitayew 2016).
All soils contain some water-soluble salts; many of them constitute plant
nutrients, but an excessive accumulation of them can cause many deleterious
effects for plant and also suppress its growth (Paul 2012, Shrivastava and Kumar
2015). It is not easy to quantify plants’ salt tolerance because it varies appreciably
with many environmental factors (soil fertility, soil physical conditions, distribu-
tion of salt in soil profile, irrigation regime, and climate) and plant factors (growth
stage, root stock, and variety of “genera, species, and cultivars”) (Juan et al. 2005;
Niu et al. 2012).
Salinity affects almost all plant development aspects including germination,
vegetative growth, and reproductive development (Bartels and Sunkar 2005).
Rahman et al. (2000) and Jamil et al. (2006) described that seed germination and
early seedling growth are the most salt-sensitive plant growth stages, because
seedling root is in direct contact with salt-affected soil. Some plants like barley,
rice, wheat, and corn showed a resistance in their first growth stages (Baniaghil et
al. 2013).
High concentration of salts in root rhizosphere badly affects plant growth
through complex interactions (Arbona et al. 2005). Salt stress affects plants in
two ways: causing water deficit referred also as “drought stress” and triggering ion
toxicity resulting from the excessive uptake of less demanded elements, mainly Cl
—
and Na+ (Setia et al. 2013; Bharti et al. 2016; Hingole and Pathak 2016).
Excessive accumulation of sodium (Na+) in cell walls can rapidly lead to osmotic
stress and cell death (Munns 2002). Uptake and accumulation of Clˉ may disrupt
photosynthetic function through the inhibition of nitrate reductase activity
(Xu et al. 2000). In rhizosphere, under excessive sodium and chloride
concentrations, there are competitive interactions with other nutrient ions (K +, NO3
—
, and H2PO4—) for binding sites and transport proteins in root cells and
partitioning within plant cells (Grattan and Grieve 1999; Tester and Davenport
2003). Once the capacity of cells to store salts is exhausted, salts build up in the
intercellular space leading to cell dehydration and death (White and Broadley
2001; Sheldon et al. 2004). Increasing salt concentrations in the environment
elevate the osmolarity outside the root zone; as the external salt concentrations
rise, cells loose water, and the water absorption becomes very difficult (Baniaghil
et al. 2013). As mentioned above, many salts are also plant nutrients, but high salt
levels in the soil can obstruct nutrient balance in plant (reducing intake N, Ca, K,
P, Fe, Zn) or interfere with some nutrients’ uptake and cause metabolic
disturbances in processes where low Na+ and high K+ or Ca2+ are required for
optimum function (Blaylock 1994; Diby and Harshad 2014). It has been stated by
Shaheen et al. (2013) that salinity stress causes perturbation in gaseous exchange
plant processes like photosynthesis, sub-stomatal CO 2 concentration, and net CO2
assimilation and transpiration rate. Salinity reduces photosynthesis capacity
mainly through complete or partial stomata closure and osmotic stress (Meloni et
al. 2003). Further, plant responses to osmotic stress are reduction in leaf area and
chlorophyll content, defoliation, and carbon assimilation reduction (Shannon and
Grieve 1999). Soil salinity significantly reduces plant phosphorus (P) uptake
because phosphate ions precipitate with Ca ions (Bano and Fatima 2009). Like
other abiotic stresses, salinity leads to oxidative stress due to increased production
and accumulation of reactive oxygen species (ROS) such as singlet oxygen,
superoxide ion, hydrogen peroxide, and hydroxyl radical on the cell, which are
detrimental to plant survival and can damage the biomembranes, proteins, nucleic
acids, and enzymes (Azevedo Neto et al. 2008; Mishra et al. 2009; Shahbazi et al.
2011). Salinity triggers alteration of metabolic processes, membrane
disorganization, reduction of cell division and expansion, and genotoxicity,
resulting in decreased growth and premature activation of programmed cell death
(PCD) (Flowers 2004; Carillo et al. 2011). Salinity adversely affects reproductive
development by inhabiting microsporogenesis and stamen filament elongation,
enhancing programmed cell death in some tissue types, ovule abortion, and
senescence of fertilized embryos (Shrivastava and Kumar 2015). It has an adverse
effect on cell cycle and differentiation; it arrests the cell cycle by reducing the
expression and activity of cyclins and cyclin-dependent kinases that result in fewer
cells in the meristem, thus limiting growth (Javid et al. 2011). Salinity can increase
the rate of ethylene biosynthesis via elevated levels of 1-aminocyclopropane-1-
carboxylic acid (ACC), which may lead to physiological changes in plant tissues
(Zapata et al. 2004; Tank and Saraf 2010). Ethylene is an important gaseous
phytohormone, which is required for many physiological processes like seed
germination, root elongation, ripening of fruit, and organ senescence (Bleecker
and Kende 2000) but up to certain concentrations (more than required level); it
acts as a negative plant growth regulator (Holguin and Glick 2001; Huang et al.
2003); it exacerbates leaf and petal abscission plus organ senescence causing early
death (Mayak et al. 2004; Cheng et al. 2007); then it acts as a stress signaling
molecule (Hahn and March 2009). It has also been reported that in various plant
species ethylene acts as a negative regulator of nodulation (Schaller 2012).
Salinity is also known to affect phytohormone synthesis, other plant growth-
stimulating factors (Xiong and Zhu 2002), protein synthesis, lipid metabolism
(Parida and Das 2005), and energy production by plants (Larcher 1980). Plants
with perturbed nutrient relations caused by salinity are more susceptible to
invasion of different pathogenic microorganisms (Romic et al. 2008).
Many studies have demonstrated that salinity inhibits seed germination of

various crops such as rice (Xu et al. 2011), wheat (Egamberdieva 2009), maize
(Khodarahmpour et al. 2012), faba bean (Rabie and Almadini 2005), soybean
(Essa 2002), cabbage, and tomato (Bojovic et al. 2010). It has been reported that
increased salinity leads to decreased root length of groundnut (Mensah et al. 2006)
and chickpea (Al-Mutawa 2003); these reports are in line with results observed by
Egamberdieva (2011), where increasing salt content reduced shoot length (50%)
and root length (7%) of bean seedling grown in a gnotobiotic sand system.
Inhibitory effect of salinity on photosynthesis has been confirmed in cowpea
(Taffouo et al. 2010) and sugar beet (Dadkhah 2011). A similar study reported an
inverse relationship between salt concentration and chlorophylls “a” and “b” and
total chlorophyll content for bean plant (Qados 2011). In basil, Golpayegani and
Tilebeni (2011) confirmed that salinity decreases photosynthesis, stomatal
conductance, chlorophyll content, and mineral uptake. In eggplant, accumulation
of Clˉ in leaves was accompanied with decreased concentration of NO3ˉ (Savvas
and Lanz 2000). Kapoor and Srivastava (2010) confirmed decrease in protein
content in black gram plants treated with different salt concentrations. In tomato,
Takagi et al. (2009) reported decreased whole plant biomass with reduced leaf
photosynthesis and transport of carbon assimilates as an effect of salinity.
2.3.3 Effect on Rhizospheric Bacteria
Even though soil microorganisms constitute less than 0.5% (w/w) of soil mass,
they play a key role in maintaining soil fertility (Tate 2000). Microbial biomass is
an important labile fraction of soil organic matter, functioning both as an agent of
transformation and recycling of organic matter and soil nutrients, by participating
in many processes such as nitrification, ammonification, nitrogen fixation, and
other ones leading to decomposition of soil organic matter and hence to the
transformation of nutrients. These microbes influence plant growth and
development directly or indirectly (Diby and Harshad 2014). Because of that, any
factor affecting the rhizospheric microbes and its functions influences the nutrient
availability and plant growth (Diby and Harshad 2014).
Salinity not only inhibits plant growth and development but also negatively
affects microbial functions and microbial biomass and changes microbial commu-
nity structure which interferes with soil fertility and reduces crops productivity
(Tripathi et al. 2007; Andronov et al. 2012), especially rhizospheric bacteria (Ofek
et al. 2006). These microbial modifications are considered as an indirect effect of
salinity on plant growth (Chowdhury et al. 2011).
Soluble salts in soil increase the osmotic potential, drawing water out of
microbial cells. As for plant roots, low osmotic potential makes it difficult for
microbes to remove water from the soil (Oren 1999). Microorganisms in
hypertonic environments (low water activity) either die or remain dormant,
lowering the activity of various degrading enzymes released by microbes and
eventually decreasing fertility (Tripathi et al. 2007; Egamberdieva et al. 2010).
Cytoplasmic membranes
of organisms are permeable to water but not to other metabolites. Therefore,

hyper- or hypo-osmotic shock exerted on cells causes a concomitant decrease or
increase in the cytoplasmic volume leading to plasmolysis and cell death (Nabti et
al. 2010). However, soil microbes can adapt to low osmotic potential. This process
is highly bioenergetically taxing, because they must maintain an osmotic
equilibrium between the cytoplasm and the surrounding medium while excluding
sodium ions from cell interior, leading to reduction in growth and activity of the
surviving microbes (Jiang et al. 2007; Ibekwe et al. 2010). In addition, the
toxicities of Na+ and other accompanying ions (Clˉ and CO32ˉ), along with very
high pH, also inhibit microbial growth and activity (Zahran 1997).
Nelson and Mele (2007) showed that sodium chloride affects the rhizosphere
microbial community structure through its influence on the quantity and/or quality
of root exudates. Nabti et al. (2010) reported that salinity inhibits bacterial
nodulation and nitrogen fixation activity by causing alteration of proteins involved
in the initial attachment steps (adsorption and anchoring) of bacteria to plant roots
in symbiotic interaction, in addition to alteration of exopolysaccharide (EPS) and
lipopolysaccharide (LPS) composition of the bacterial cell surface, impairment of
molecular signal exchange between bacteria and their plant host due to the
alteration of membrane glucan contents, and inhibition of bacterial mobility and
chemotaxis toward plant roots. Singleton and Bohlool (1984) have also
demonstrated the disturbance effect of symbiotic interaction between legumes and
rhizobia by soil salinity. Rabie et al. (2005) reported decrease in nodulation and
nitrogen fixation with reduced nitrogenase activity in legumes such as soybean,
common bean, and faba bean. High salinity inhibited nitrogen fixation at the level
of nifH gene expression and nitrogenase activity in Azospirillum sp. (Tripathi et
al. 2002). Some studies showed that soil respiration decreased with increasing soil
salinity (Yuan et al. 2007; Wong et al. 2009; Setia et al. 2010). Many enzyme
activities such as urease, amylase, invertase, catalase, alkaline phosphatase, and β-
glucosidase were strongly inhibited by salinity (Frankenberger and Bingham 1982;
Ghollaratta and Raiesi 2007; Pan et al. 2013). With an increase in the salinity level
above 5%, the total count of bacteria and Actinobacteria were drastically reduced
in studies conducted by Omar et al. (1994) and Wichern et al. (2006).
2.4 Halotolerant PGPRs as a New Strategy to Alleviate

Salt Stress in Plant
It must be noticed that salinity is one of the major abiotic stresses affecting plant
growth and productivity in arid and semiarid regions (Yadav et al. 2011); it is an
important growth-limiting factor for most non-halophytic plants. According to
FAO, more than 831 million hectares of land are affected by salinity throughout
the world (Martinez-Beltran and Manzur 2005).
Moreover, a number of authors observed that salt effect on growth of different
crops such as pepper, tomato, soybean, wheat, canola, and lettuce was alleviated
by using halotolerant PGPRs. Similarly, it was reported that PGPRs’ increased
shoot and
Fig. 2.1 Effect of PGPRs inoculation on wheat plant growth under nonsaline and saline
conditions. Plants were grown in soil under glasshouse conditions and supplemented with
150 mM NaCl through irrigation and harvested 60 days after germination. (Bharti et al. 2016)
root length and dry weight of soybean (Naz et al. 2009) and wheat (Fig. 2.1)
(Bharti et al. 2016) under salt stress. P. extremorientalis TSAU20 and P.
chlororaphis TSAU13 were shown to improve growth of various crops under
saline conditions (Egamberdieva and Kucharova 2009). Jha and Subramanian
(2013) cited the role of PGPRs in the regulation of ion concentration, nutrient
uptake, and antioxidant enzymes in plant cultivated under salt stress. Moreover,
the results obtained by Sapsirisopa et al. (2009) revealed that treatments of rice
with Bacillus megaterium A12ag significantly increased N and P content in
shoots. PGPR strains can also enhance chlorophyll, carotenoid, nitrogen, and
phosphorus concentrations in plant (Jha and Subramanian 2013; Saghafi et al.
2013). In addition, co-inoculation with Azospirillum lipoferum and Pseudomonas
fluorescens increases meaningfully chlorophyll a and b and carotenoid contents
in wheat (Saghafi et al. 2013); similar results were also reported by Nadeem et al.
(2006) who showed that inoculation of maize seeds with rhizobacterial strains
augmented chlorophyll a and b and carotenoid contents of fresh leaves at 10 dS m
—1
. On the other hand, PGPRs can induce antioxidant enzyme production in salt-
stressed plant, which is an essential mechanism to detoxify reactive oxygen
species (ROS). Kumar et al. (2003) and Jha and Subramanian (2013) reported that
the antioxidant activity is more significant when PGPRs are present. PGPR
application could also increase seed germination; it is the case of inoculation with
P. pseudoalcaligenes and Bacillus pumilus showing an increase of paddy seed
germination under saline conditions (Jha and Subramanian 2013). Likewise, they
showed that B. megaterium A12ag improved significantly the rice seed
germination at EC 10 dS/m. The same strain had similar effect on tomato seeds at
NaCl concentration between 30 and 90 mM. It also augmented seedling dry
weight at NaCl up to 120 mM (Chookietwattana and Maneewan 2012).
Due to their promising effect on plant growth under saline stress, the use of
PGPRs is becoming prevalent worldwide. In addition to alleviating salinity stress
in
Table 2.1 Salinity stress alleviation by PGPR species in various crops

PGPRs Crops Effect References
Brevibacterium epidermidis Canola Enhanced plant growth and Siddikee et al.
RS15, Micrococcus reduced level of ethylene (2010)
yunnanensis RS222, and
Bacillus aryabhattai RS341
Rhizobium and Pseudomonas Mung Improved plant growth and Ahmad et al.
bean increased salt tolerance index of (2013)
plant
Pseudomonas putida R4 and Cotton Improved seed germination and Egamberdieva
P. chlororaphis R5 seedlings growth and alleviated et al. (2015)
salt stress in cotton seedlings
Dietzia natronolimnaea STR1 Wheat Promoted salinity tolerance of Bharti et al.
plant and enhanced gene (2016)
expression of antioxidant
enzymes
Bacillus megaterium and Okra Improved plant growth, Habib et al.
Enterobacter sp. increased antioxidant enzyme (2016)
activities, and upregulated ROS
pathway genes
Bacillus sp. Wheat Improved shoot and root length Orhan (2016)
Bacillus mojavensis K78 Wheat Improved plant growth, Pourbabaee
increased chlorophyll content et al. (2016)
and nutrient uptake, and reduced
levels of ethylene
Agrobacterium tumefaciens and Peanut Enhanced plant growth, Sharma et al.
Pseudomonas sp. maintained ion homeostasis, (2016)
and reduced reactive oxygen
species (ROS) level
Bacillus cereus Y5, Bacillus sp. Wheat Improved plant growth Khan et al.
Y14, and B. subtilis Y16 (2017)
plants (Table 2.1), several reports suggest that PGPRs can also enhance plant
tolerance toward other abiotic stresses such as drought (Sandhya et al. 2009;
Timmusk and Wagner 1999), chilling injury (Barka et al. 2006), metal toxicity
(Dell’ Amico et al. 2008; Bensidhoum et al. 2016), and elevated temperature stress
(Ali et al. 2009).
2.4.1 Mechanisms of Plant Promotion by Halotolerant

PGPRs in Saline Soil
Potential of halotolerant PGPRs to increase crop productivity under stressful envi-

ronment involves various mechanisms. These are similar to those implicated in
halosensitive bacteria for plant growth promotion under elevated salinity. These
mechanisms are summarized in Fig. 2.2.
2.4.1.1 1-Aminocyclopropane-1-carboxylic Acid (ACC) Deaminase

Ethylene is a gaseous plant hormone involved in plant growth and development as
well as in plant response to a wide range of abiotic and biotic stresses (Abeles et
al. 1992). The presence of ethylene may be stimulatory or inhibitory depending on
its concentration, the nature of the physiological process, and the growth phase of
plant (Shaharoona et al. 2006). Under stress conditions such as salinity, plant
hormone ethylene endogenously regulates plant homoeostasis resulting in reduced
root and shoot growth (Shrivastava and Kumar 2015; Vurukonda et al. 2016). A
number of PGPRs promote plant growth by lowering stress ethylene
concentrations through their 1-aminocyclopropane-1-carboxylic acid (ACC)
deaminase enzymes (Glick 1995; Penrose et al. 2001; Glick 2014). This enzyme
can hydrolyze the endogenous levels of ACC, which is an immediate precursor of
ethylene biosynthesis in plants, into ammonia and α-ketobutyrate resulting in
reduced level of ethylene (Hontzeas et al. 2004; Glick et al. 2007; Nascimento
et al. 2014; Santoyo et al. 2016; Khan et al. 2017). PGPRs producing this enzyme
protect plant from deleterious effect of salinity and drought (Glick et al. 1998;
Saleem et al. 2007; Zahir et al. 2009). By studying the role of ACC deaminase
enzyme-producing bacteria, numerous authors reported the implication of ACC
deaminase in promoting growth and health status of plant growing in salt-affected
soils. El-Tarabily et al. (2008) showed that ACC deaminase producing Streptomy-
ces filipinensis 15 and S. atrovirens 26 can positively influence plant growth by
reducing tomato endogenous ACC levels in both roots and shoots. Similarly,
ethylene production by tomato seedlings was reduced by the bacterium
Achromobacter piechaudii as reported by Mayak et al. (2004). They revealed the
significant increase of fresh and dry weights of tomato grown in NaCl (up to
172 mM). Nadeem et al. (2006) have also mentioned that inoculation of canola by
ACC deaminase producing P. syringae and Pseudomonas sp. improves yield and
growth under salinity (12 dS m—1). ACC deaminase-containing PGPRs enhance
chlorophyll contents of canola, lettuce, as well as maize (Glick et al. 1997; Han
and Lee 2005; Nadeem et al. 2006). Saravanakumar and Samiyappan (2007)
exhibited that P. fluorescens containing ACC deaminase activity enhanced saline
resistance in groundnut plants and increased yield as compared to Pseudomonas
strains lacking ACC deaminase activity. The role of PGPRs containing ACC
deaminase in improving nodulation in legumes has been demonstrated by
Shaharoona et al. (2006) showing that inoculation with PGPR containing ACC
deaminase promoted nodule formation by indigenous competitive
Bradyrhizobium. Thereby, these bacteria could be a promising approach for
successful nodulation in legumes (Zafar-ul-Hye et al. 2013).
2.4.1.2 Phytohormone Biosynthesis

Plant hormones play a crucial role in controlling the way in which plants grow and
develop (Davies 1995). The commonly recognized classes of phytohormones,
regarded as the “classical five,” are the auxins, gibberellins, cytokinins, abscisic
acid, and ethylene (Baca and Elmerich 2007). It is well documented that the most
important mechanisms adopted by PGPRs to improve plant growth involve
phytohormone production, which can control several plant growth parameters and
development both under normal and stressed environment. Numerous authors
showed that salt stress affects negatively endogenous levels of phytohormones.
Indeed, exogenous application of plant growth regulators alleviated salt effect in
several plants, e.g., wheat (Nabti 2007; Egamberdieva and Kucharova 2009),
maize (Khalid et al. 2013; Kaya et al. 2013), cotton (Egamberdieva et al. 2015),
and mung bean (Ahmad et al. 2013). Indole-3-acetic acid (IAA) is one of the most
important phytohormones that regulate many aspects of plant growth and develop-
ment, e.g., cell division, seed germination, differentiation of tissues, leaf expan-
sion, root elongation, and resistance to stressful conditions (Egamberdieva 2008;
Maleki et al. 2010; Martínez-Viveros et al. 2010). Egamberdieva et al. (2015)
reported that IAA-producing bacterial strains P. putida R4 and P. chlororaphis R5
improved seed germination up to 64 and 73% in response of NaCl stress. These
two strains have significantly increased root and shoot length of cotton seedling at
100 mM NaCl compared to the uninoculated seedlings. Khalid et al. (2013)
reported also the role of exogenous application of IAA in alleviating the deleteri-
ous effect of salt stress in maize plant. It was found that IAA-overproducing
PGPR strains are able to alleviate different stress conditions by increasing proline
amount in Medicago plants (Saghafi et al. 2013). The ability of halotolerant
bacteria to modulate plant stress level by producing IAA was previously reported
for bacteria isolated from halophyte root in Argentina (Sgroy et al. 2009), coastal
soil (Siddikee et al. 2010), rhizosphere of C. annuum growing in desert areas
(Marasco et al. 2012), and Salicornia plant rhizosphere (Mapelli et al. 2013).
Besides its role in stimulating plant growth, IAA produced by PGPRs can be
absorbed by plants, and in combination with endogenous plant, IAA can stimulate
ACC synthase (Penrose and Glick 2001; Gerhardt et al. 2006). This enzyme
converts S-adenosylmethionine (SAM) to ACC which is the immediate precursor
to ethylene (Kende 1993). Much of this ACC is exuded from seeds and roots
then taken up by PGPRs and subsequently converted by ACC deaminase to
ammonia and α-ketobutyrate (Glick et al. 1998; Penrose 2000; Holguin and Glick
2001; Gerhardt et al. 2006). Therefore, ACC reduction leads to lowering ethylene
content in plant, thus alleviating the inhibitory effect of high ethylene
concentration on plant development (Fig. 2.2). High concentration of IAA, which
reflects a higher synthesis rate of ACC, might result in a negative impact on root
growth and seed germination (Siddikee et al. 2011; Nakbanpote et al. 2014).
Siddikee et al. (2010) revealed that halotolerant bacteria producing both ACC
deaminase and IAA enhance root elongation and dry weight of canola to a greater
extent than the strains producing solely ACC deaminase. Glick et al. (2007)
suggested that IAA and ACC deaminase stimulate root growth in a coordinated
fashion. Since IAA stimulates ACC production which is converted into ethylene
and since ACC deaminase hydrolyzes ACC and decreases ethylene level, the final
ethylene effect or root growth depends on the balance of IAA and ACC deaminase
(Arora et al. 2012). Certainly as cited by Glick (2014), synergy between ACC
deaminase- producing bacteria and IAA is indispensable to enhance plant growth
and development under salt stress.
Fig. 2.2 Mechanisms involved by PGPRs to alleviate salt stress in plant. (a) ACC deaminase
enzyme produced by PGPR reduces the ethylene level in plant. ACC 1-aminocyclopropane-1-
carboxylic acid, IAA indole-3-acetic acid, SAM S-adenosyl methionine, ROS reactive oxygen
species
2.4.1.3 Induced Systemic Tolerance (IST): Antioxidant Enzymes

As sessile organisms, plants are frequently exposed to several biotic and abiotic
stresses. The application of PGPRs may help plant to cope with these two types of
stress. Unlike direct mechanisms involved by PGPRs to improve plant growth
(e.g., phytohormones synthesis, phosphate solubilization, and nitrogen fixation),
indirect mechanisms lead to protect plant from both biotic and abiotic stress. Jha
and Saraf (2012) suggested that PGPRs can induce defense programs such as
systemic acquired resistance (SAR) and induced systemic resistance (ISR), thus
reducing phytotoxic microbial communities. Recently, many studies about the role
of PGPRs in eliciting plants to tolerate abiotic stresses, e.g., drought, salt, cold,
and high temperature, were published. The term “induced systemic tolerance”
(IST) was proposed for PGPRs that induced physical and chemical changes in
plants that result in enhanced tolerance to abiotic stresses (Mantelin and Touraine
2004). Among the mechanisms involved by PGPR plant tolerance induction under
salt stress, antioxidant enzymes can be mentioned.
Under abiotic stress such as salinity, plant can suffer from membrane damage
due to the generation of reactive oxygen species (ROS) including superoxide
radical (O2—), hydroxyl radical (OH—), and hydrogen peroxide (H2O2) which
causes oxidative damage to biomolecules such as lipids and proteins and
eventually leads to plant death (Del Rio et al. 2003). Perturbation of the cellular
redox state is adjusted by the activation of antioxidant system in plant (Gill and
Tuteja 2010; Jha and Subramanian 2013), by production of antioxidant enzymes,
e.g., superoxide dismutase (SOD), peroxidase (POX), and catalase (CAT), and
nonenzymatic antioxidants such as ascorbate, glutathione, and a-tocopherol (Del
Rio et al. 2003). Numerous reports were edited recently on the ability of PGPRs to
activate plant antioxidant machinery and to reduce salt stress. Han and Lee (2005)
mentioned the ability of PGPRs to induce antioxidant enzymes in lettuce; they
said that the inoculation with two PGPR strains, Serratia sp. and Rhizobium sp.,
into saline soils alleviated salinity effects on the antioxidant enzymes ascorbate,
peroxidase (APX), and glutathione reductase (GR). Kohler et al. (2009) showed
that the induction of antioxidant enzymes by PGPR strains increased the tolerance
of lettuce grown under sever salt stress. PGPR strain Bacillus cereus Pb25
increased significantly antioxidant enzyme (POD, SOD, and CAT) activities in
Vigna radiata (mung bean) (Islam et al. 2015). To monitor the putative changes in
the expression of genes encoding the ROS-scavenging enzymes, Gururani et al.
(2013) subjected the PGPR-inoculated and non-inoculated potato plants to
different stresses. They showed that the mRNA expression of SOD and APX, in
bacteria-inoculated plants growing under stress conditions, increased con-
siderably in comparison to non-inoculated stressed plants. Similarly, mRNA
expression levels of genes encoding for other antioxidative enzymes such as
CAT and GR also increased in bacteria-treated plants. Therefore, inoculation with
selected PGPRs could serve as a useful tool for alleviating oxidative stress in
plants. According to Bharti et al. (2016), salt-stressed plants applied with
halotolerant PGPR showed an improvement in gene expression levels as compared
to uninoculated salt-stressed plants. They noticed that shoot of APX, CAT, and
POD of PGPR-inoculated salt- stressed plants recorded a threefold increase in
gene expression as compared to
uninoculated non-stressed plants. Plants’ salt-stressed roots inoculated with

PGPRs recorded a two- to threefold increase in gene expression of antioxidants in
comparison with the non-stressed control plants.
2.4.1.4 Ion Homeostasis and Nutrient Uptake

Salt stress affects plant development either through perturbation of water balance
or imbalance in ratio of ion homeostasis. Numerous reports showed that salinity
increased Na+ accumulation and consequently decreased Ca+ and K+ uptake
(Yildirim et al. 2006; Zhang et al. 2008; Tank and Saraf 2010; Shukla et al. 2011;
Rojas-Tapias et al. 2012; Aamir et al. 2013; Jha and Subramanian 2013; Younesi
et al. 2013; Sharma et al. 2016). Accumulation of toxic ions (Na+ and Cl—)
perturbs water balance and ion homeostasis, which eventually disturbs metabolic
processes and hormonal status and affects enzymes, photosynthetic function,
transpiration, and translocation of nutrients (Munns 2002). Maintenance of low
Na+/K+ is one of the predominant mechanisms involved by PGPRs to improve
plant growth under high salinity (Munns and Tester 2008). They have the ability
to increase mineral nutrient exchange and to alleviate nutrient imbalance caused
by the high influx of Na+ and Cl— ions. According to Hamdia et al. (2004) and
Ilangumaran and Smith (2017), PGPRs promote growth of salt-affected plant by
changing the selectivity of cation (Na +, K+, and Ca+), maintaining a higher K +/Na+
ratio, reducing Na+ and Cl— accumulation in leaves, increasing Na+ exclusion via
roots, and boosting the activity of high-affinity K+ transporters. Several authors
highlighted the PGPRs’ role in reducing Na+/K+ ratio in plant under salt stress.
Peanut seedlings treated with three isolates (MBE01, MBE02, and MBE05)
showed lower shoot Na+/K+ ratio than non-inoculated seedlings under salinity
stress (Sharma et al. 2016). Han and Lee (2005) showed that PGPR strains
increased the tolerance of maize plant by lowering Na+/K+ ratio. Plants inoculated
by PGPR strains Brachybacterium saurashtrense and Brevibacterium casei
achieved the maximum-reduced Na+ concentration in addition to the Na+/K+ ratio
lowered at both 0 and 100 mM NaCl (Shukla et al. 2011). Salt stress affects also
gene expression involved in ion homeostasis. Pinedo et al. (2015) clarified the
deleterious effect of salt stress on the expression of ion homeostasis-related gene
(Arabidopsis K+ transporter 1, high-affinity K+ transporter 1, sodium hydrogen
exchanger 2, and Arabidopsis salt overly sensitive 1). They displayed that PGPR
strain Burkholderia phytofirmans PsJN regulates the expression of important ion
homeostasis-related genes after short- and long-term exposure to salt stress. A
tissue-specific regulation of HKT1 by the soil bacterium B. subtilis GB03 confers
salt tolerance in Arabidopsis thaliana. Under salt stress, this strain concurrently
downregulates HKT1 expression in roots and upregulates its expression in
shoots, resulting in lower Na + accumulation throughout the plant compared to the
control (Zhang et al. 2008). Recently, Niu et al. (2015) reported that B. subtilis
GB03 strain upregulated PtSOS1 gene expression under salt stress (200 mM
NaCl), which is consistent with improved salt tolerance and reduced Na +
accumulation in shoots, roots, and whole plants of P. tenuiflora.
Salinity reduces plant nutrient uptake, which leads to reduction of plant growth
and development. Salt stress causes competitive interactions between toxic ions
and
nutrient ions for binding sites and transport proteins in root cells and thereafter for
translocation, deposition, and partitioning within the plant (Tester and Davenport
2003). Consequently, to this interaction, the concentration of nutrient elements
will be reduced in whole plant. Numerous researches exhibited the PGPR ability to
provide plants with nutrient elements under salt stress (Yildirim et al. 2006; Zhang
et al. 2008; Shukla et al. 2011; Aamir et al. 2013; Jha and Subramanian 2013; Niu
et al. 2015; Sharma et al. 2016). Jha and Subramanian (2013) found that plant
inoculated by PGPR strains increased N, P, and K concentration and reduced that
of Na and Ca. Similarly, Aamir et al. (2013) observed that N, P, and K
concentration and protein content in grain increased by inoculation and co-
inoculation with Rhizobium and plant growth-promoting rhizobacteria.
2.4.1.5 Osmoprotective Compounds: Compatible Solutes

Under salt stress and to be adapted to the fluctuation in osmolarity, bacteria apply
two main strategies: “salt in” mechanism and production of organic osmolytes
(Korcan et al. 2015; Mohammadipanah et al. 2015), which is the major
mechanism involved by both prokaryote and eukaryote organisms to alleviate salt
stress. The osmoadaptation strategy in halophilic and halotolerant bacteria consists
on the accumulation of K+ ions and glutamate (first response) (Sleator et al. Hill
2001; Le Rudulier et al. 2002); if the osmotic shock persists or increases, bacteria
accumulate compatible solutes (second response) (Lucht et al. Bremer 1994;
Bartlett et al. Roberts 2004). Compatible solutes are so named because, even at
high concentration in the cytoplasm, they do not interfere with the vital cellular
processes (Kempf and Bremer 1998) and they can be synthesized by halophiles
organisms or accumulated by uptake from surrounding medium
(Mohammadipanah et al. 2015). These organic osmolytes harbor different classes
of molecules including amino acids and their derivatives (proline, glutamate,
glutamine, ectoine, and taurine), sugars (sucrose, trehalose), methylamines
(glycine betaine), and polyols (mannitol, erythritol, and glycerol) (Oren 2002;
Yancey 2005). The presence of halotolerant bacteria in saline soils may play an
important role in interaction with plants (Nabti et al. 2015). They can improve
plant growth by realizing these molecules in medium. Such organic compounds,
taken up and accumulated by plants unable to synthesize them de novo and able to
improve growth under inhibitory osmolarities, are called osmoprotectants. Thus,
the concept of osmoprotectant supposes an ecological cycle in which compatible
solutes are transported from producers to consumers injured by osmotic stress
(Arora et al. 2012). A number of studies on halophilic and halotolerant PGPRs
demonstrated their ability to increase compatible solutes in plants under stress
conditions. Sandhya et al. (2010) observed that Pseudomonas strain GAP 45
increased compatible solutes and antioxidant status of maize plants under water-
stressed conditions. Proline accumulation is a very common response in plants
exposed to abiotic stress. Saghafi et al. (2013) showed that PGPR strains increased
proline contents in wheat cultivars. Similarly, Naz et al. (2009) reported that
PGPR isolates increase significantly proline contents of shoots and roots of
soybean plant under salt stress. It was noted that Medicago plant inoculated by
IAA-overproducing PGPR strain is able to cope with different stress conditions
and
accumulates high level of proline (Saghafi et al. 2013). Increased proline and total
soluble sugar contents in the PGPR-treated wheat plants contributed significantly
to their osmotolerance (Upadhyay et al. 2012). Similarly, trehalose metabolism in
rhizobia also seems important for improving plant growth, yield, and adaptation to
abiotic stress of leguminous plants (Suarez et al. 2008). In addition to their ability
to restore plant growth by providing compatible solutes, halotolerant PGPRs can
improve plant growth under salt stress by the same mechanisms used by PGPRs in
normal conditions.
2.5 Halotolerant PGPR Algae: A Promising

Consortium to Alleviate Salt Stress in Plant
The mechanisms used by PGPRs to improve plant growth and health under salt
stress can be inhibited or weakened if these bacteria are unable to overcome this
stress. As reported previously, the accumulation of exogenous compatible solutes
protects and stimulates bacterial growth in hyperosmotic environment. Compatible
solute accumulation by uptake from the medium is preferred over biosynthesis,
since uptake is energetically less expensive than biosynthesis (Imhoff 1986). Nabti
et al. (2010) highlighted that bacteria belonging to the genus Azospirillum
accumulate compatible solutes such as glutamate, proline, glycine betaine, and
trehalose in order to adapt to salt stress.
By their composition rich in phytohormones, polysaccharides, nutrient
elements, and vitamins, algae can protect and improve plant growth in normal and
stressed environment. Besides, they are the major source for compatible solute for
plant and bacteria in a stressed environment. Ghoul et al. (1995) showed that algal
extracts contain high amount of compatible solutes as betaines, amino acids, and
DMSP. They noticed that algal extracts convey significant osmoprotection to E.
coli under salt stress. Tolerance to NaCl of A. brasilense NH was increased up to
600 mmol/l in the presence of glycine betaine and Ulva lactuca extracts (Nabti et
al. 2007). Pichereau et al. (1998) demonstrated also the role of algae to stimulate
bacterial growth in a stressed environment, by their organic osmolytes GB (N, N,
N-trimethylglycine) and 3-dimethylsulfoniopropionate (DMSP) which acts as
osmoprotectants. Few studies have been performed on the role of the consortium
algae/PGPRs in plant growth stimulation. These studies consist of the
simultaneous application of PGPRs and algae extracts under stress conditions,
where the algae extracts were used as source of osmoprotectants. The main role of
this combination is to restore bacterial growth and improve their interaction with
plants and thus ameliorates plant productivity in stressed environment. As reported
by Nabti et al. (2007), algal extracts enhance bacteria performance and thus
support their plant growth-promoting effect. Arif (2016) showed that Ulva lactuca
extracts restored germination, biomass, chlorophyll contents, and protein of wheat
inoculated by
P. fluorescens under salt stress. Similarly, Nabti et al. (2007) exhibited that the
PGPR strain A. brasilense restored wheat growth under salt stress even better in
the presence of Ulva lactuca extracts.
2.6 Conclusion
Improvement of plant growth in saline soils by inoculation with halotolerant

PGPRs could be a good solution as a suitable alternative to improve crop growth
and yield in this hostile environment. Furthermore, these bacteria showed a high
capacity to enhance plant growth under saline conditions by using multiple and
variable mechanisms, such as the strategy of osmoregulation. In addition,
stimulation of plant growth in saline soils seems to involve the same mechanisms
like other halosensitive bacteria.
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Halotolerant Rhizobacteria: A Promising
Probiotic for Saline Soil-Based Agriculture 3
Ankita Alexander, Avinash Mishra, and Bhavanath Jha
Abstract
Soil salinity is a serious threat to sustainable agriculture, and a number of research
are going on to improve saline-resistant crops by using various breeding
methods and genetic engineering tools. These methods are time-consuming,
often face yield penalties, and many other ethical issues. There is a need to
explore other more stable, environmentally friendly methods for the sustainable
agriculture. Exploration of plant growth-promoting rhizobacteria (PGPR)
associated with salt-tolerant plants (halophytes) and their use as probiotics for
saline soil agriculture are a promising substitute for classical approaches.
Salinity is one of the major abiotic stress reported from arid and semiarid
regions which causes a major loss in the agriculture productivity. Halophytes
are adapted to the saline environment because of their genetic makeup and
associated microbiome. These microbiomes have potential to survive in the
saline condition, but they are not thoroughly explored. Several studies showed
that bacteria associated with halophytes, directly and indirectly, support the
plant growth and yield in saline conditions; thus, these bacteria can be used as
probiotics for salt-sensitive plants (glycophytes) grown in the salt-affected area
to enhance the productivity. PGPR induce many morphological, physiological,
and genetic changes in a plant which compensate the pressure of salt stress. The
genetic level changes in plants due to application or the presence of PGPR are
known as induced systemic resistance (ISR). PGPR secrete some beneficial
elements like organic solutes, siderophores, etc. to survive in harsh
conditions. PGPR also help plants to maintain their
A. Alexander · A. Mishra (*) · B. Jha (*)

CSIR-Central Salt and Marine Chemicals Research Institute, Bhavnagar, Gujarat, India
Academy of Scientific and Innovative Research, Council of Scientific and Industrial Research,
Ghaziabad, India
e-mail: [email protected]; [email protected]

54 A. Alexander et al.
osmotic pressure and nutrient balance. The presence of PGPR also affects the
level of various phytohormones in plants which play a major role in growth,
development, and stress response of the plant.
Keywords
Halophytes · Salt-sensitive plants · Halotolerant PGPR · Salinity stress · Crop
plants
3.1 Introduction
As human probiotics, plant-probiotic microorganisms (PPM) are beneficial

microorganisms which can act as bio-protectants (reduce pathogen infection), bio-
fertilizers (increase yield), and biostimulants, additionally also reduce various biotic
and abiotic plant stresses (de Souza Vandenberghe et al. 2017). According to
FAO/WHO expert consultation report, probiotics are “live microorganisms which
when administered in adequate amounts confer a health benefit on the host” (Hill et al.
2014).
Plant growth is affected by various abiotic factors like abundance of heavy
metals, soil toxicity, salinity, cold, drought, temperature and flood. Among these,
soil salinity is a major cause which adversely affects the plant growth and produc-
tivity (Príncipe et al. 2007). The soil is considered saline when electrical
conductivity (EC) of the saturation extract of the rhizosphere soil (root zone)
exceeds 4 dS m—1 which is equivalent to approximately 40 mM NaCl at 25 ○C;
commonly, a higher EC limits the crop productivity (Munns and Tester 2008).
Primary salinization is caused by the salts that are already present in the soil, and
secondary salinization is a result of excessive use of chemical fertilizers, soil
amendments, and inadequate irrigation management (Carillo et al. 2011).
According to reports of FAO (2016), 20% of total agriculture land has been
severely affected by excessive soil salinity.
Soil salinity adversely affects the plant health at a physiological, biochemical,
and molecular level which decreases the growth and yield of crop plants (Roy et
al. 2014). The development of salt stress-resistant transgenic plants is considered
as an option for saline soil agriculture; however, there is a need for
environmentally friendly, ethical, and natural procedure for sustainable agriculture
(Ashraf 2009). Halophytic plant species are adapted to saline soils, naturally.
These plants can survive in this harsh environment by their specific genetic
makeup and their root-associated microbiome having very diverse rhizobacteria
(Mishra and Tanna 2017; Mukhtar et al. 2017). Rhizobacteria isolated from
microbiome of halophytes may help the glycophytic plant to grow in saline soil
and enhance the productivity of glycophytic crop plants. These rhizobacteria can
be used for the improvement of the soil quality.
3 Halotolerant Rhizobacteria: A Promising Probiotic for Saline Soil-Based.. . 55
3.2 Effect of Salt on Plant Growth
Plant growth is affected by salt at multiple levels. The primary effect of soil
salinity on plant growth and productivity is briefly discussed as follows:
3.2.1 Osmotic Stress
During stress, water intake by root is very difficult which results in reduced
transpiration rate and leaf expansion, stomatal closure, water retention, water use
efficiency, and increased rate of senescence of older leaves (Munns and Tester
2008). Osmotic stress also leads to the production of reactive oxygen species
(ROS) which results in autophagy (Han et al. 2011).
3.2.2 Nutrient Imbalance
Soil salinity profoundly influences the nutrient imbalance and causes nutrients
deficiency in plants (Blaylock 1994). In saline soil, it is difficult to take
phosphorus
(P) because phosphate ions precipitate with Ca ions and become unavailable for
plant utilization (Bano and Fatima 2009).
3.2.3 Decrease in Photosynthesis
Salt stress damages the photosynthetic capability of the plant. During salt stress,
growth of the plant is affected, and it also causes a reduction in leaf area,
degradation of chlorophyll and carotene content, low level of stomatal
conductance, and harmful effects on PSII and PSI which altogether result in the
decrease of photosynthesis ability of plant (Netondo et al. 2004).
3.2.4 Effect on Reproductivity
Salinity badly disturbs reproductive machinery of the affected plant. Salt stress
inhibits microsporogenesis (formation of microspores), floral development, ovule
abortion, embryo arrest, and senescence of fertilized embryos, but induces
apoptosis (programmed cell death) in some reproductive tissues (Shrivastava and
Kumar 2015).
3.2.5 Ion Toxicity
Ion toxicity is the major problem of soil salinity. During salinity, excess sodium
ion causes leaf burn and defoliation (Podmore 2009). Chloride toxicity causes
leaf
bronzing and necrotic spots in plant species (Rahnama et al. 2010). A high level of
Cl— disturbs NO3— uptake in leaves which results in the decrease of nitrate
reductase (NR) activity, affecting the nitrogen assimilation in plants (Baki et al.
2000). Excessive salt causes replacement of K + by Na+ which promotes
conformational changes in many proteins and enzymes, and these affect many
metabolic and molecular alterations in plants (Zhu 2002; Chinnusamy et al. 2006).
3.2.6 Oxidative Stress
Salinity induces the generation of reactive oxygen species (ROS) and free radicals
which causes oxidative stress and reduces the level of antioxidant enzymes such as
catalase (CAT), superoxide dismutase (SOD), peroxidase (POX), glutathione
(GSH), ascorbate peroxidase (APX), glutathione reductase (GR), glutathione-S-
transferase (GST), and monodehydroascorbate reductase in plants (AbdElgawad
et al. 2016). ROS are harmful to cell components and damage lipids, protein, and
nucleic acids; furthermore, long-term exposure causes the death of host species
(del Rio et al. 2003).
3.2.7 Production of Excess Ethylene
Plants, when subjected to salinity, produce excessive ethylene, which severely

retards root development (Mahajan and Tuteja 2005). Under biotic and abiotic
stress conditions, ethylene causes a decrease in root growth and senescence in
crop plants (Ma et al. 2003). In general, salt stress adversely affects the cell cycle
and differentiation by reducing the expression and activity of cyclins and cyclin-
dependent kinases. Some reports also showed that salinity also reduces seed
germination, seedling growth, and enzyme activity (Seckin et al. 2009), which
ultimately affects plant yield.
3.3 Need for Plant Probiotic
For the sustainable agriculture toward biotic and abiotic stress, transgenic
approaches are commonly used, but there are many shortcomings and limitation of
transgenic plants. These approaches need a long time and need much manpower
from lab to field and after that have less success rate (Coleman- Derr and Tringe
2014). Transgenic approaches caused unstable progeny due to the involvement of
multiple genes in abiotic stress responses and also the uncertainty of gene flow in
the next generation (Jewell et al. 2010). Transgenic crops are facing the difficulty
of public acceptance as well as many ethical issues (Fedoroff 2010). Molecular
techniques which are involved in the development of transgenic crops are most of
the time not applicable or responsive in case of tetraploid and hexaploid species.
Saline and alkaline stresses are typically linked in nature (Saslis-Lagoudakis et al.
2014), and the tolerance of
transgenic toward high soil alkalinity (pH) and/or salt alkaline-mixed conditions
could not fully obtain (Yamaguchi and Blumwald 2005). Sometimes transgenic
salt-tolerant crops, especially in which transcription factors have been genetically
modified, resulting in the low yield of the plant (Roy et al. 2014). When a plant is
facing salt stress, many genes, proteins, and metabolites are activated at the same
time, but transgenic plants are concentrated on either only one gene or one
promoter only, so protection against salt stress is not obtained completely or up to
desired level (Bhatnagar-Mathur et al. 2008).
To overcome these problems and for the fulfillment of increasing food demand
in an environment-friendly manner, there is a need of exploring more useful
alternative strategies for sustainable agriculture. The health of the plant and its
response toward any stress are affected by not only its genome but also
microbiome of its surround- ings (Munns and Gilliham 2015; Vannier et al. 2015).
Plant root system releases a large number of nutrients, known as rhizodeposits
(e.g., exudates, border cells, and mucilage). Rhizodeposits influence the
rhizosphere by regulating the microbial diversity and activity on plant roots (Cook
et al. 1995). The rhizosphere is a narrow zone of soil including surrounding plant
roots and it can contain up to 1011 microbial cells per gram of the root
(Egamberdieva 2008).
The microbes have coevolved with their corresponding hosts and adapted their
community structure for specific environmental stresses (Lau and Lennon 2012).
Thus, interacting network among root, soil, and microorganisms plays an
imperative role in supporting healthy growth and defense mechanism under
unfavorable conditions (biotic and abiotic stress) for both the host and its
associated organisms. Some of these microbes support their host plant regarding
growth, yield, in biotic and abiotic stress (Fig. 3.1). Due to plant growth-
promoting traits of these bacteria, they are called plant growth-promoting bacteria
(PGPB), and PGPB which are found in the rhizosphere and stimulate plant growth
are called plant growth-promoting rhizobacteria (PGPR) (Kloepper and Schroth
1981). PGPR can be classified as extracellular and intracellular. Extracellular
PGPR (ePGPR) exist in the rhizosphere, on the rhizoplane, in the spaces between
root cortex cells, while intracellular PGPR (iPGPR) exist inside root cells,
generally in specialized nodules (Gray and Smith 2005).
3.4 Rhizobacteria as Probiotic
The term induced systemic tolerance (IST) has been proposed for PGPR-induced
physical and chemical changes that result in enhanced abiotic stress tolerance
(Shrivastava and Kumar 2015). Halotolerant rhizobacteria have many
characteristics which improve the plant health (Fig. 3.2), including nitrogen
fixation, phosphate solubilization, production of phytohormones and
exopolysaccharide, aminocyclopropane-1-carboxylate deaminase (ACCD)
production, and biolytic enzyme secretion (de Souza et al. 2015).
Long time exposure

Retarded growth plant Enhanced growth and yield of plant
Chlorophyll loss and

necrotic patches Ion-exclusion
Transpiration rate mechanisms
Photosynthesis Phytohormones
Production
Osmolyte production
Generation of ROS
Activated ISR
Stress
Root development
Nutrients accessibility ACCD activity
Excessive ethylene Siderophores Ethylene level

production
P and Fe uptake Biocontrol N2 fixation
√
No PGPR
Fig. 3.1 Role of PGPR in the plant growth promotion
Fig. 3.2 Probiotic activity of PGPR for plant growth promotion

3.4.1 ACCD Activity
Many halotolerant bacterial isolates showed the ACCD activity which required for
plant health (Santoyo et al. 2016). Plants naturally select ACCD-producing
bacteria under stress conditions. PGPR produce the enzyme ACC deaminase
which cleaves the plant ethylene precursor ACC into ammonia and α-ketobutyrate
and decrease the level of ethylene in seedlings and plants. Additionally, ACCD
stimulates IAA production and thus enhances the growth and survival of plant
under abiotic stress (Glick 2014; Mayak et al. 2004a, b).
3.4.2 Osmolyte Production
Osmolytes are highly soluble substances with no net charge at physiological pH,
so they do not interact with proteins and compatible with many cellular functions
such as DNA–protein interactions, protein–protein interactions, cellular
metabolism, and osmotic balance (Lippert and Galinski 1992; Welsh 2000). The
most studied osmolytes, produced and secreted by halotolerant PGPR, are
trehalose, glucosylglycerol (GG), proline, glycine betaine, and choline (Qurashi
and Sabri 2013). Trehalose is nonreducing disaccharide which is not common in
vascular plants but acts as an osmoprotectant. It stabilizes dehydrated enzymes
and membranes, thus protects them from desiccation. Trehalose metabolism is
important for plant growth, and yield of leguminous plants under abiotic stress
conditions (Suarez et al. 2008). Stenotrophomonas rhizophila is halotolerant
rhizobacteria which can grow at 4% NaCl and produce the trehalose in response to
salt stress (Roder et al. 2005).
3.4.3 Ion-Exclusion Mechanisms
Rhizobacteria can alter root uptake of toxic ions by slight changes in the
physiology of host plant (by regulating ion transporters) and by modification in
physical barriers around the roots (Siddikee et al. 2011) or by directly reducing
accumulation of toxic ions (Na+ and Cl—). Rhizobacteria also improve the
nutritional status of the plant by maintaining the essential level of both macro (N,
P, and K) and micronutrients (Zn, Fe, Cu, and Mn). Zahir et al. (2009) showed
higher K+/Na+ ratios in salinized crop plants like wheat after inoculation with
Pseudomonas and Serratia sp.
3.4.4 Increment in Nutrients Accessibility
Phosphorus (P) is abundantly available in soils in both organic and inorganic form,
but it is not easily available for plants because the majority of soil P is found in
insoluble forms. Microbial-induced changes in rhizosphere pH (organic acid
excretion) convert insoluble phosphorus in soil into the soluble state (El-
Tarabily and
Youssef 2010). In soil, iron occurs as Fe3+ and forms insoluble hydroxides which
becomes inaccessible to plants. PGPR also secret some organic molecules called
as siderophores. These siderophores help plants to take iron because they chelate
Fe3+ (Rajkumar et al. 2010). It is shown that siderophores produced by
Enterobacter sp. 638 and Pseudomonas sp. enhance the growth of poplar and
tomato, respectively (Taghavi et al. 2009; Nishma et al. 2014).
3.4.5 N2 Fixation
Nitrogen fixation is the process of conversion of atmospheric N 2 to NH3.

Microorganisms involved in N2 fixation are rhizosphere associated either
symbiotic or endophytic. Rhizosphere-associated bacteria use carbon compounds
from root exudates for N2 fixation. All these microorganisms contain specific
genes for N2 fixation, for example, a nifH gene that encodes for dinitrogenase
reductase enzyme which converts N2 to NH3 and makes it available for plants
(Raymond et al. 2004).
3.4.6 Production of Phytohormones
Rhizobacteria also produce a variety of phytohormones like cytokinin, indole-3-

acetic acid (IAA), abscisic acid (ABA), and gibberellic acid (GA) (Glick 2012).
Phytohormones produced by PGPR play an important role in increasing root
surface area, and numbers of root tip in many plants, thus increasing the
accessibility of plants to soil nutrients (Narula et al. 2006). Similarly, GA
enhances the shoot growth and total biomass of the plant (Boiero et al. 2007).
ABA regulates the stomatal activity of plants hence indirectly affects the
photosynthesis response to the saline soil (Dodd 2003). Many PGPR, isolated
from saline soil, produced ABA which can enhance the growth of plants under
saline condition (Naz et al. 2009).
3.4.7 Biocontrol Agent
PGPR also secret some antibiotic compounds which play a major role in the
reduction of phytopathogens and deleterious rhizobacteria (Stutz et al. 1986). By
acting as a biocontrol agent, rhizobacteria stimulate plant growth indirectly. They
synthesize extracellular enzymes to hydrolyze the cell wall of pathogens and com-
pete with harmful bacteria for niches within the rhizosphere (Zahir et al. 2004; van
Loon 2007). PGPR also activate induced systemic resistance (ISR) in host plant to
fight with pathogens at the molecular level (Chandler et al. 2008).
3.5 Halotolerant Rhizobacteria
Bacteria which are associated with halophytic plants can tolerate salt level up to
4–30% (Yuan et al. 2016) and play an essential role in the survival of halophytes
in the harsh environment and are called as halophyte rhizosphere-associated
microbes (HRAMs). These bacteria are endowed with specific metabolic signals
which are essential for plant’s survival under salt stress (Szymanska et al. 2013).
The plant– microbes interaction effectively improves the soil quality and fertility
(Yuan et al. 2016). HRAMs have all PGPR activity with high salt tolerance, so
they are the most suitable candidate for growth and yield enhancement in
glycophytic plants in salt- affected areas in most environmentally friendly manner.
3.6 Halotolerant Bacteria as Plant Probiotics for Saline Soil-

Based Agriculture
Proper osmotic regulation is a crucial point for plants growing in the saline area;
the absence of this results in loss of turgidity, cell dehydration, failure of
photosynthetic machinery, nutritional disorders, toxicities, less crop productivity,
and ultimately death of cells (Ashraf 2004; Shrivastava and Kumar 2015).
Halotolerant bacteria survive under salt stress conditions because they modify
the osmolality of the rhizosphere (Egamberdieva 2011). These modified osmolytes
are made available for utilization of plant and act as free radical scavengers, a
regulator of the photosynthetic apparatus, and stabilizer of subcellular structures
(Yang et al. 2009), hence affecting the plant growth (Miller and Wood 1996), so,
they are considered as an effective candidate for plant growth promotion.
Previously, many studies showed that halotolerant PGPR are capable to amelio-
rate the detrimental effect of salinity on the growth of basil, canola, maize, and
tomato plants (Kang et al. 2014; Rojas-Tapias et al. 2012). Karuppasamy et al.
(2011) showed that the growth of tree legumes Samanea saman could be
improved by the application of stress-tolerant rhizobia. Halotolerant bacterial
consortia isolated from avocado trees could ameliorate salinity stress in other plant
species such as wheat (Barra et al. 2016). Upadhyay et al. (2009) isolated 130
rhizobacterial strains from the rhizosphere of wheat plants grown in a saline zone
and showed that out of 130, 24 were tolerant to relatively high levels (up to 8%) of
NaCl. All of the 24 salt-tolerant isolates were able to produce IAA, 10 isolates
solubilized phosphorus, eight isolates produced siderophores, 6 were involved in
gibberellin production, and 2 isolates contained the nifH gene, which indicates
that the whole consortia have PGPR ability. In another study, Nadeem et al.
(2010) evaluate a number of axenic cultures of rhizobacterial strains for their
plant–growth potential under varying salinity stress conditions. At a high salinity
level (15 dS m—1), the PGPR–inoculants improved overall plant growth including
plant height, root length, plant biomass, and also grain yield by 37%, 70%,
116%, and 111%, respectively. It was also observed that treated plants also
had higher K+/Na+ ratios, relative water, and chlorophyll contents along with lower
proline contents. Potential halotolerant rhizobacteria reported for
sustainable saline soil agriculture are listed in Table 3.1.
Table 3.1 Potential halotolerant rhizobacteria with different plant growth-promoting traits
Plant growth-
promoting trait
Name of bacteria Isolated from observed References
Achromobacter Rhizosphere of arid Increase in the Mayak et al.
piechaudii ARV8 and saline biomass of tomato (2004a, b)
environment seedlings under salt
stress
Bacillus pumilus, Rhizosphere of 30 Production of indole- Upadhyay et al.
B. aquimaris, days old wheat 3-acetic acid (IAA), (2009)
B. arsenicus, plants grown in a phosphorus
B. sporothermodurances, saline zone solubilization,
Arthrobacter sp., siderophore
B. cereus, Pseudomonas production,
medicona, and B. subtilis gibberellin
production, and the
presence of nifH gene
Acinetobacter, Rhizobacteria Improved plant Egamberdieva
Alcaligenes faecalis, isolated from wheat growth and nutrition (2008)
Bacillus cereus, and pea grown in under salt stress
Enterobacter hormaechei, loamy sand soil
Pantoae, and
Pseudomonas aeruginosa
Stenotrophomonas Highly salinated soils Increase of Egamberdieva
rhizophila strain germination rate, (2011)
DSM14405T shoot, and root
growth of wheat,
tomato, lettuce, sweet
pepper, melon,
celery, and carrot
Bacillus megaterium Degraded soil Increase in root Marulanda et al.
hydraulic (2010)
conductance in Zea
mays
Pseudomonas mendocina Rhizosphere Enhanced growth and Kohler et al.
nutrient uptake of (2009)
Lactuca sativa
Azotobacter chroococcum Rhizosphere Enhanced oxidative Stajner et al.
stress tolerance in (1997)
sugar beet
Pseudomonas putida Alkaline soil Increased the K+/Na+ Yao et al.
Rs-198 ratios (2010)
Consortia of plant growth- Rhizosphere of Increase in salt Naz et al.
promoting rhizobacteria weeds (Chrysopogon tolerance in Glycine (2009)
aucheri, Lactuca max L.
dissecta, Solanum
surattense, and
Sonchus arvensis)
grown in saline soils
Bacillus pumilus with Root tissue of rice as Induction of Jha et al. (2011)
P. pseudoalcaligenes well as the osmoprotectant and
(continued)

Plant growth-
promoting trait
rhizospheric soil of antioxidant proteins
rice in paddy
Azospirillum strains Saline or non-saline Increased shoot dry Nia et al. (2012)
soil weight and grain
yield in wheat
Halobacillus sp. and Rhizosphere of saline Ameliorated salt Ramadoss et al.
Bacillus halodenitrificans habitats stress in wheat (2013)
seedlings and
increased root length
Virgibacillus marismortui Dessert soil Improved the stem Essghaier et al.
and Terribacillus growth in tomato (2014)
halophilus
Promicromonospora sp. Field soil sample Improved growth of Kang et al.
SE188 Solanum (2012)
lycopersicum
Group of rhizobacteria Roots of Salicornia Increased plant Mapelli et al.
grown in hypersaline growth (2013)
soils
Bacillus subtilis, Rhizosphere of plants Promoted yield and Karlidag et al.
B. atrophaeus, naturally grown high growth of strawberry (2010) and
B. spharicus, salty soils and lettuce under Yildirim et al.
Staphylococcus kloosii saline conditions (2011)
and Kocuria Erythromyxa
Zhihengliuella Salt-affected soils Improved growth in Orhan (2016)
halotolerans, Triticum aestivum
Staphylococcus succinus, L. under salt stress
Bacillus gibsonii,
Oceanobacillus
oncorhynchi, Halomonas
sp., and Thalassobacillus
sp.
Azospirillum spp. Mangrove Growth promotion in Bashan et al.
rhizosphere Salicornia bigelovii (2000)
Endophytic bacteria Roots of halophyte Growth promotion in Piernik et al.
Pseudomonas sp. ISE-12 Salicornia europaea Beta vulgaris under (2017)
and Xanthomonadales saline conditions
sp. CSE-34
Consortia od Roots of coastal sand Increase in plant Shin et al.
rhizobacteria mainly dune plants growth (2007)
Pseudomonas sp.
Klebsiella oxytoca Rs-5 Salinized cotton Salt stress relief and Yue et al.
fields growth promotion in (2007)
cotton
Pseudomonas aeruginosa Rhizosphere of Plant growth Tewari and
PF23 different plants promotion, Arora (2014)
biocontrol, and stress
(continued)

Plant growth-
promoting trait
amelioration in
sunflower under
saline conditions
Bacillus, Pseudomonas, Roots of halophyte Stimulated the Qin et al. (2014)
Klebsiella, Serratia, Limonium sinense growth of the
Arthrobacter, Limonium sinense
Streptomyces, seed germination and
Isoptericola, and seedling growth
Microbacterium under salinity stress
Novosphingobium Rhizosphere of Increase in growth of Krishnan et al.
pokkalii sp. nov saline-tolerant pokkali rice plants (2017)
pokkali rice (VTL-2 variety)
Bacillus sp. and Rhizospheric soil and Growth of Palacio-
Pseudomonas lini roots of Distichlis Arabidopsis thaliana, Rodríguez et al.
spicata Cucumis sativus, and (2017)
Citrullus lanatus
Enterobacter asburiae, Acacia arabia grown Alleviation of salt Raheem and Ali
Bacillus thuringiensis, in a saline soil stress of Triticum (2015)
Moraxella aestivum
pluranimalium, Bacillus
thuringiensis, and
Pseudomonas stutzeri
Flavobacterium Agricultural sites Remarkable Abdelwahab
johnsoniae, Pseudomonas used for wheat enhancement in et al. (2017)
putida, Achromobacter cultivation germination of wheat
xylosoxidans, and seeds
Azotobacter chroococcum
Azospirillum brasilense Rhizosphere of many Alleviation of saline Khalid et al.
kinds of grasses stress in Trifolium (2017)
repens
Montagnulaceae sp. Rhizosphere of Plant growth Yuan et al.
Jp-root-44 halotolerant seep promotion of (2016)
weed Suaeda salsa Cucumis sativus and
Oryza sativa in
normal and in salt
stress
Pseudomonas syringae Rhizosphere and Improved total dry Ahmad et al.
and Pseudomonas nodules of mung weight and salt (2013)
fluorescens in different bean grown in salt- tolerance of mung
combination of affected fields bean
Rhizobium strain
Enterobacter sp. EJ01 Rhizosphere soil of Promoted growth and Kim et al.
Dianthus japonicus,a increased the salt (2014)
halophyte, in resistance of tomato
reclaimed land seedlings
(continued)

Plant growth-
promoting trait
Brevibacterium Rhizosphere of six Enhanced growth of Siddikee et al.
epidermidis RS15, different naturally canola seedlings (2010)
Micrococcus yunnanensis grown halophytic under saline stress
RS222, and Bacillus plants of the saline
aryabhattai RS341, coastal region
Pseudomonas Rhizosphere of Enhanced fresh Tank and Saraf
fluorescens, tomato plants grown weight as well as dry (2010)
P. aeruginosa, and in agricultural land weight of tomato
P. stutzeri when grown in the
presence of salt
Cellulosimicrobium sp. Salt-affected Increase in growth of Nabti et al.
S16 agricultural barley seedlings as (2014)
rhizospheric soil well as increase in
biological control
abilities
Bacillus pumilus, High saline habitats Induced salt tolerance Tiwari et al.
Pseudomonas mendocina, in Triticum aestivum (2011)
Arthrobacter sp., L.
Halomonas sp., and
Nitrinicola lacisaponensis
Hartmannibacter Rhizosphere of Increase in growth of Suarez et al.
diazotrophicus Plantago winteri Hordeum vulgare (2015)
from a natural salt under salt stress
meadow
Azospirillum brasilense Rhizosphere of salt- Enhanced growth of Nabti et al.
affected wheat field durum wheat (2010)
soil (Triticum durum var.
waha) under saline
soil conditions
Streptomyces isolate Rhizosphere of wheat Increase in growth Sadeghi et al.
and development of a (2012)
wheat plant in normal
and saline conditions
Alcaligenes faecalis, Soils from root region Positive impacts on Bal et al. (2013)
Bacillus pumilus, and of rice grown in different growth
Ochrobactrum sp. coastal soils parameters of rice
under salinity stress
Bacillus subtilis and Rhizosphere of 30 Alleviation of the Upadhyay et al.
Arthrobacter sp. days old wheat adverse effects of soil (2012)
plants grown in a salinity on wheat
saline zone growth
Azospirillum sp. Nonsaline and saline Positive impact on Zarea et al.
soil wheat seedlings (2012)
Pseudomonas Saline areas Growth promotion in Patel et al.
pseudoalcaligenes and chickpea under saline (2012)
P. putida stress
(continued)

Plant growth-
promoting trait
Pseudomonas sp. Rhizosphere soil Facilitated growth of Fu et al. (2010)
samples of eggplants eggplants seedlings
(Solanum melongena under salt stress
L.) grown in the
coastal saline soil
Bacillus sp. and Saline soils Growth promotion of Príncipe et al.
Ochrobactrum sp. Zea mays and (2007)
Agropyron
elongatum under
salinity conditions
Pseudomonas fluorescens Rhizosphere of Enhanced the saline Saravanakumar
coastal and forestry resistance in and
ecosystems groundnut plants Samiyappan
(2007)
Azospirillum Maize rhizosphere Enhanced growth of Hamdia et al.
two cultivars of (2004)
maize in saline stress
Micrococcus Saline habitats at the Enhanced salt stress Zhou et al.
yunnanensis, edge desert tolerance remarkably (2017)
Planococcus rifietoensis, in Beta vulgaris L.
and Variovorax
paradoxus
Consortia of Rhizospheric soils of Ameliorated the Barra et al.
Enterobacter, Serratia, avocado trees located effect of salt (NaCl) (2016)
Serratia, Pseudomonas, near the sea stress on the
Microbacterium and emergence, growth,
Achromobacter, and biomass of wheat
seedlings
Pseudomonas Soil of the root zone Significantly Egamberdiyeva
alcaligenes, of melon enhanced plant and Hoflich
P. denitrificans, Bacillus growth and nutrient (2004)
polymyxa, and uptake in cotton and
Mycobacterium phlei pea in the pot
experiments
Bacillus megaterium and Crop fields Increase in salinity Habib et al.
Enterobacter sp. stress tolerance in (2016)
okra
Achromobacter Arid and saline Increased in the Mayak et al.
piechaudii ARV8 environment biomass of tomato in (2004b)
saline stress
Pseudomonas putida, Saline soil Enhanced the Nadeem et al.
Enterobacter cloacae, germination (2013)
Serratia ficaria, and percentage,
Pseudomonas fluorescens germination rate in
wheat at high salinity
3.7 Conclusion
Halotolerant rhizobacteria-based agriculture is more efficient and environment-

friendly than plant breeding and modification at the genetic level. The plant
microbiome is considered as a pan–genome (second plant genome) having the
capability to enhance host stress tolerance. It is well established that multiple plant
growth-promoting traits are present in the bacterial communities of a halophytic
rhizosphere. A number of halotolerant bacteria were isolated from the rhizosphere
of halophytes, and their potential was studied to enhance plant growth under saline
environments. Although single PGPR strain can enhance plant growth and
tolerance to abiotic stress, several reports suggest that plants often supported by
more than a single type of symbiotic microbe to combat salinity. A co-culture
system containing two or more microbes is proven to be more efficient for the
plant health. However, the use of PGPR in agriculture needs more extensive
research and awareness. In addition to the study on plant physiology or
microbiome of the host plant, it is also needed to concentrate on plant-microbe
interaction to understand the whole mechanism during biotic and abiotic stress.
Identification of the plant–microbes exudates, plant–microbes signals, and key
players in the rhizosphere microbiome will provide unique metabolic and
physiological markers which can elucidate the mechanism of plant–growth
promotion by PGPR, additionally can also reveal whether and how plants recruit
and stimulate beneficial (micro)organisms or its result of any stress.
Acknowledgment CSIR-CSMCRI Communication No.: PRIS-42/2018.
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Development of Salt Tolerance in Crops
Employing Halotolerant Plant Growth– 4
Promoting Rhizobacteria Associated
with Halophytic Rhizosphere Soils
Ashok Panda and Asish Kumar Parida
Abstract
Increasing levels of salinity in agricultural lands is one of the most serious
environmental concerns that pose a risk to the food security of the growing
human population of the world. According to the United Nations Environment
Program, the total areas of salt-stressed agricultural lands and croplands have
increased by approximately 20% and 50%, respectively, worldwide. The total
land area that cannot be used as agricultural land is increasing by 1–2% every
year as a result of soil salinization, mostly in dry areas. Increasing soil salinity
is becoming the prime reason for substantial decreases in agricultural yield due
to inhibitory effects of salinity on growth, photosynthesis, protein synthesis,
lipid metabolism, and many other metabolic processes of plants. Production of
salt- tolerant crop varieties is a prerequisite for meeting increasing food
demands and creating sustainable agriculture practices. The halophytic
rhizosphere is a reservoir of plant growth–promoting rhizobacteria (PGPRs),
which can enhance plant adaptation and growth under high salinity. Among
free-living soil bacteria, PGPRs play an essential role in promoting plant
growth even in stress conditions. PGPRs have both direct and indirect effects
on plant growth. The direct mechanisms involve biosynthesis of
phytohormones, enhanced nitrogen fixation, and higher levels of phosphate
solubilization. The indirect mechanisms involve inhibition of phytopathogens
that reduce plant growth. Various studies have illustrated that salinity-tolerant
PGPRs obtained from rhizosphere soils of various halophytic species have
potential for use in development of glycophytic salt- tolerant crops in salt-
dominated agricultural lands through their use as
A. Panda · A. K. Parida (*)

Division of Biotechnology and Phycology, Council of Scientific and Industrial Research–Central
Salt and Marine Chemicals Research Institute (CSIR-CSMCRI), Bhavnagar, Gujarat, India
Academy of Scientific and Innovative Research, Council of Scientific and Industrial Research–
Central Salt and Marine Chemicals Research Institute (CSIR-CSMCRI), Bhavnagar, Gujarat,
India e-mail: [email protected]; [email protected]

76 A. Panda and A. K. Parida
bioinoculants. To accomplish this goal, PGPRs adapt various mechanisms such

as modulation of phytohormones, gene expression, protein function, and metab-
olite synthesis. PGPRs modulate synthesis of 1-aminocyclopropane-1-
carboxylate (ACC) deaminase along with indoleacetic acid (IAA), which
function in stress signaling and induce various stress-responsive pathways.
Implementation of PGPR inoculation in the advancement of agriculture to
increase global food security is desirable. This chapter focuses on the salinity
tolerance mechanisms of PGPRs and the roles of PGPRs in developing salt
tolerance in various glycophytic crop species.
Keywords
ACC deaminase · Halophyte · IAA · PGPR · Phytohormones · Salinity · Salt-
tolerant crop · Siderophore
4.1 Introduction
Salinization now affects more than one billion hectares of land worldwide and is
considered a serious environmental threat to many coastal countries
(Egamberdieva and Lugtenberg 2014). The major factors responsible for the
increase in salinity are poor agricultural practices, irrigation with saline water, and
low precipitation. Gradual decreases in the availability of fresh water result in use
of salt water for irrigation (Egamberdieva and Lugtenberg 2014).
Natural salinity is defined as addition of salt to the soil or surface water bodies
by natural means. Intrusion of salt water into coastal lands and deposition of salt
by winds are the major natural sources of salt accumulation (Manchanda and Garg
2008). Moreover, addition of salts to agricultural land from the ocean occurs
through transfer by winds or by rainfall precipitation of ocean water. In addition,
salt can be added to soil by weathering of mineral rocks (Paul and Lade 2014).
Anthropogenic causes of increasing soil salinity include excessive irrigation
with saline water, which makes most agricultural land unfit for agriculture by
increasing the level of dissolved salts (Egamberdieva and Lugtenberg 2014). Other
causative factors include excessive supplementation with inorganic fertilizers and
various changes in the soil structure. All of these factors continuously contribute
to land degradation, representing a large burden on natural ecosystems (Paul and
Lade 2014). The main impacts of high soil salinity are degradation of the soil
structure through excessive accumulation of Na+ along with deterioration of the
hydraulic properties of the soil. Apart from this, high levels of soil Na+ tend to
increase the soil pH and increase soil erosion. Most importantly, Na + plays a
decisive role in destruction of other clay minerals by dispersion. The process of
dispersion occurs through replacement of Ca2+ and Mg2+ in the inner layer of soil
coagulates by intruding Na+ (Paul and Lade 2014). Agricultural lands with less
rainfall and higher temperatures due to extreme climate change convert into saline
land more rapidly.
4 Development of Salt Tolerance in Crops Employing Halotolerant Plant Growth... 77
This results in occurrence of more arid regions, favoring even more salt accumula-
tion (Shanker and Venkateswarlu 2011). As mentioned earlier, salinization is
defined as accumulation of different kinds of salt ions, including magnesium (Mg2
+
), potassium (K+), chloride (Cl—), calcium (Ca2+), carbonate (CO32—), sulfate (SO42
—
), sodium (Na+), and bicarbonate (HCO3—). Consequently, the total area of land
that is affected by salinity and the total area of abandoned agricultural land are
increasing day by day (Paul and Lade 2014). Salinity stress generates reactive
oxygen species (ROS), which damage DNA, RNA, and proteins (Habib et al.
2016). ROS also cause decreases in chlorophyll levels and the activity of root
meristems, hindering root growth. On the other hand, various antioxidant enzymes
such as superoxide dismutase (SOD), catalase (CAT), and ascorbate peroxidase
(APX) have the ability to scavenge ROS and maintain the level of ROS within the
tolerance limit (Jaleel et al. 2009). SOD is a metalloenzyme that protects cells and
various cellular organs from damage caused by oxidative stress, by neutralizing
superoxide radicals. APX plays a significant role in breakdown of H2O2 produced
by SOD. Furthermore, H2O2 produced by the action of SOD is neutralized by
catalase into H2O and O2 (Habib et al. 2016).
Development of salinity-tolerant crops is becoming a more desirable scientific
achievement in view of the increase in soil salinity in agricultural lands and the
decrease in the rate of agricultural productivity due to salinization. Well-organized
soil management practices, which involve efficient cost management and formula-
tion of methods that are easily adaptable, are a challenge that must be met for
successful reclamation of saline soils (Munns and Tester 2008). In addition, in
contrast to conventional agriculture, it is essential to institute sustainable manage-
ment practices that provide more support to meet the future needs of agriculture.
Various microorganisms that play helpful roles in agriculture in an eco-friendly
manner have been shown to be of great benefit (Rodriguez and Redman 2008).
Moreover, various researchers have demonstrated that the associations between
rhizospheric microbes and stressed plants help the plants to adapt to their microen-
vironment (Paul and Lade 2014). A variety of agricultural crops grown at a wide
range of salinity levels have been shown to respond to such rhizospheric
microorganisms, which enhance the growth of these crops. This approach make it
possible to develop salinity-tolerant varieties of crops, although this was
previously believed to be impossible. Stress alleviation in crops that are habituated
to saline soils occurs by implementation of beneficial rhizobacteria that colonize
the rhizosphere soil of the plants. Successful implementation of this approach is
possible because of the wide range of tolerance of these microorganisms, their
productive interactions with plants, and use of prospective implementation
methods. The percentage of rhizobacteria in inoculations that generally play
beneficial roles in plant growth under adverse environmental conditions is about
2–5%. Plant growth– promoting rhizobacteria (PGPRs) make soil ecosystems
nutrient rich and make crop yields sustainable (Hayat et al. 2010). The various
ways in which microbes stimulate plant growth and alleviate stress responses
include (1) efficient nutrient mobilization in the soil, (2) protection from
phytopathogens, and (3) improvement of soil structure and quality by
sequestration of toxic heavy metals. Microbes can also aid degradation of various
xenobiotic compounds (Braud et al. 2009).
Use of microbial inoculants for improving plant health in salinized soils holds
promise for amelioration of salt stress and promotion of plant growth, along with
improvement of disease resistance (Lugtenberg et al. 2013). Bacterial species that
are closely associated with plant roots are of immense importance in alleviating
the effects of stress and opening up new opportunities for development of
technologies for salinity tolerance (Dodd and Pérez-Alfocea 2012). Earlier reports
documented the usefulness of microbes in plant responses to various
environmental extremes such as drought, soil and surface water salinity, and
heavy metal stress. These kinds of approaches supports development of
sustainable agricultural practices. Preinoculation of the germplasms of different
crops such as pepper, tomato, and beans with PGPR strains tends to increase the
plant biomass as well as the yield, reflecting enhanced tolerance of prevailing
salinity.
4.2 Effects of Salinity on Plant Physiology
Optimal plant growth and agricultural yields are affected by salinity in many crops
(Paul and Lade 2014). Various plants such as cereals, pulses, and other
horticultural crops are greatly affected by prevailing salinity either in irrigation
water or in the soil solution. Reports have documented decreased seed germination
rates in response to salinity in wheat (Egamberdieva 2009), faba beans (Rabie et
al. 2005), rice (Xu et al. 2011), maize, and soybean (Essa 2002). Reduced water
uptake and improper mobilization of essential nutrients may be the reasons for the
reduction in growth in response to salinity (Dolatabadian et al. 2011).
Mobilization of some essential macronutrients in plants is affected by abundance
of Na+ and Cl— ions in the rhizospheric region (Heidari and Jamshid 2010). Major
physiological pathways such as protein synthesis, photosynthesis, and lipid
metabolism are altered by the onset of salinity. The rate of carbon assimilation
declines because prevailing salinity induces an osmotic imbalance and stomatal
closure (Parida and Das 2005). The overall effects of osmotic stress in plants
include a significant decrease in cell growth, a reduction in leaf area, chlorophyll
degradation, and, most importantly, senescence (Paul and Lade 2014). The effects
of salinity are multivariate, including hormonal and ionic imbalances, alterations
in protein metabolism, and a decline in the enzyme activity that is responsible for
nucleic acid metabolism. These morphological and physiological anomalies are
attributable to osmotic imbalance and toxicity of salt ions. Apart from Na+, Cl—
also disturbs the plant’s regular physiology (e.g., photosynthesis). Excessive
accumulation of these two ions in the rhizosphere induces competitive absorption
of other mineral ions such as K+, NO3—, and H2PO4 in the roots along with
competition for translocation and for tissue-specific localiza- tion. Intake of salts
by plants beyond their tolerance (storage capacity) leads to storage of ions in the
intercellular spaces, which causes dehydration and death of plant tissues. Salinity
affects the osmotic balance of root cells, which becomes lower than that in the
surrounding rhizosphere solution, and this, in turn, influences water and nutrient
uptake. Various primary effects of salinity tend to have various secondary
consequences such as osmotic imbalance, oxidative stress, and ROS
accumulation, leading to disintegration of membranes or other macromolecules.

Implementation of both enzymatic and nonenzymatic antioxidant systems confers
protection against stress-induced oxidative damage. In addition, the levels of
expression of these antioxidant molecules can be used as indicators of the extent
of oxidative stress in plants.
4.3 Impacts of Salinity on Rhizospheric Microbiodiversity
The microbial colony in the rhizosphere is an indispensable and dynamic element

of soil composition, and it functions as an agent for recycling of nutrients as well
as for transformation of organic matter to provide nutrients for optimum growth of
the plants. Most microorganisms colonize the plant rhizosphere, rather than the
surrounding soil, because of its favorable environment. The microbes in the rhizo-
sphere soil have significant influences on the survival of plants in direct and
indirect ways. As the microbial community modulates the nutrient availability to
the plants, any alterations in the community as a result of environmental factors
influence the nutrient supply to plants from the soil. Increased microbial
populations in the rhizosphere have many effects, particularly in proper
functioning of the ecosystem, pollutant degradation, and decontamination of
contaminated environments (Wenzel 2009). The rhizospheric microbial
community structure is affected by soil sodium chloride, influencing root exudates
(Nelson and Mele 2007). The density of microbes such as Pseudomonas species
has been reported to be significantly decreased by salinity in the rhizosphere of
rice. A number of Pseudomonas species are habituated to saline soil; these include
P. stutzeri, P. fluorescens, P. aeruginosa,
P. putida, and P. mendocina (Egamberdieva and Lugtenberg 2014). The salt-
tolerant nitrogen-fixing bacterium Swaminathania salitolerans has been obtained
from rice associated with mangroves (Loganathan and Nair 2004). Apart from
Pseudomonas species, various salt-resistant rhizobacteria such as
Serratia marcescens,
P. aeruginosa, and Achromobacter xylosoxidans have been reported to be present
in the rhizosphere of rice. Similarly, various reports have suggested that the rhizo-
sphere of salt-grown wheat is a potential PGPR reservoir (Egamberdiyeva and
Islam 2008). It is evident from the consistent presence of P. aeruginosa in saline
soils that this species is widespread in the rhizosphere soil of salt-grown plants.
Microorganisms and plants compete for the available nutrients. Beneficial bacteria
are attracted to the plants by secretions from roots in the rhizospheric zone. To
survive in a saline environment, microbes have to expend extra energy for mainte-
nance of the osmotic balance between both sides of their plasma membranes and
also have to exclude Na+ (Jiang et al. 2007). In saline conditions, plants use most
of the available rhizospheric osmolytes, depriving microbes of those osmolytes
and restricting bacterial growth. Salinity affects the composition of protein,
lipopolysaccharides, and exopolysaccharides present on the bacterial surface. In
addition, salinity affects the arrangement of membrane glucans that regulate
signaling on the bacterial surface, affecting the mobility of bacteria (Ibekwe et al.
2010). An alteration in bacterial diversity is one of the biomarkers for
determination of
salinity effects on the quality of soil. Moreover, early detection of salinity in soil
can be helpful for implementation of remedial action to improve crop survival and
yield (Ibekwe et al. 2010). Halotolerant rhizobacteria implement an array of
adaptive measures to maintain survival and growth under high salinity. Their
adaptive mechanisms include (1) modification of the structural texture of the cell
membrane and cell wall to minimize salt uptake; (2) efficient osmotic adjustment
through regulation of intracellular ion concentrations by K+/Na+ ion transporters
and Na+/ H+ antiporters; (3) endogenous biosynthesis of trehalose, sucrose,
glycerol, and glycosyl, which serve as compatible solutes; (4) biosynthesis of
enzymes that can withstand high salinity; and (5) production of biofilms composed
of exopolysaccharides (Sandhya et al. 2010b; Qin et al. 2016). Besides these
mechanisms, other features of salt-tolerant rhizobacteria such as higher guanine–
cytosine (GC) content, high levels of low hydrophobic proteins, less formation of
helices, and higher levels of stabilized coil structures may enhance their
halotolerance characteristics (Szymańska et al. 2016).
4.4 Salt Tolerance Mechanisms of Rhizospheric PGPRs
Microorganisms belonging to the domains of Bacteria and Archaea have the

unique property of maintaining cellular integrity in response to changes in the
osmolarity of the external soil solution. It was discovered that apart from the
members of the Halobacteriaceae family, other species are also adaptable to high
levels of NaCl (Oren 2002). Lately, it has been suggested that apart from archaea,
the prokaryotic diversity in high-saline environments also includes different
species of bacteria. This hypothesis has been further supported by isolation of a
wide array of salt-tolerant bacteria at all latitudes. Salt-tolerant bacteria can grow
on plant parts pickled in a salt solution; for example, Staphylococcus xylosus was
found on plant parts soaked in a salt solution containing ~7.2% NaCl (Abou-Elela
et al. 2010). Bacterial genera such as Nesterenkonia, Stenotrophomonas, and
Litoribacter have been found in a saline area of northeast China (Shi et al. 2012),
and Mesorhizobium alhagi has been found in the northwestern desert of China
(Zhou et al. 2012a). High salinity can be withstood by avoidance of high
cytoplasmic salt concentrations and water loss through specific cell wall
construction and composition, which are known to be particular characteristics of
archaea and cyanobacteria. The highly resistant lipid membranes of archaea,
which are resistant to temperature and mechanical anomalies, make these species
salt tolerant. In comparison with eukaryotes, the lipid membranes of archaea make
them better suited to harsh environmental conditions for better survival. The cell
walls of some members of Halobacteriales contain an S-layer made up of
glycoprotein, which is arranged in a two-dimensional lattice. The membranes are
made up of about 40–50% glycoprotein and are stabilized by the presence of
NaCl. In a similar way, the cyanobacterial membrane system contains a two-
membrane structure, i.e., an inner membrane and an outer membrane. The outer
membrane encloses the periplasmic space, and the inner membrane surrounds the
cytoplasmic content. Another membrane system is present in chloroplasts as
thylakoid membranes, which accommodate the photosynthetic complexes and the

electron transport chain (Ruppel et al. 2013). Apart from this, the coccoid
Natronococcus occultus has been reported to have a thick cell wall, which requires
a certain amount of salt for its structural integrity. The integrity of the wall of
Halococcus, which is made up of poly(L-glutamine) glycoconjugate, differs
greatly depending on the presence or absence of salt. In addition, several
rhizobacterial species secrete salinity stress alleviator exopolysaccharides
(Upadhyay et al. 2011). The role of these polysaccharides in reducing salt stress
was demonstrated in Nostoc sp. The presence of salt in the growth media did not
alter the composition of the wall in terms of the ratio of sugars in comparison with
the control media (Yoshimura et al. 2012). The intracellular ionic concentration is
maintained by various ion channels, resulting in osmotic adjustment. The level of
Na+ in the cell is kept low by a proton electrochemical gradient using Na+/H+
antiporters. The essential role of K+ includes maintenance of membrane integrity
and energetics, pH regulation, and, most importantly, regulation of gene
expression (Hagemann 2011). Both Na+ and K+ have the same chemical and
physical properties. Na+ has the same-sized hydration shell as K +; hence, it
competes with K+ uptake and causes K+ deficiency in plants. In contrast, an
optimum level of K+ in the intracellular matrix suggests uninterrupted K + uptake
from the soil solution (Hagemann 2011).
4.5 PGPRs Isolated from Different Halophytic Rhizospheres
Microorganisms that are associated with soil and a halophytic rhizosphere

influence the growth and development of plants both beneficially and
detrimentally. The growth of plants inoculated with PGPRs can be altered directly
and/or indirectly. For soil microorganisms the plant rhizosphere is a favored
ecological niche because of rich nutrient availability. The maximum activity of
beneficial bacteria is mainly accomplished in the rhizosphere. This is because of
the attractants and nutrients secreted in the form of different organic compounds
from the roots, attracting an array of bacterial species (Szymańska et al. 2016).
Beneficial effects on plants are exerted by various soil microorganisms, and
sustainable crop production is procured by opposite effects on soilborne pests.
Adverse conditions make microorganisms more tolerant and make them potential
candidates for use in various environmental stress conditions along with salinity.
Nevertheless, the diversity and growth of various bacterial species are affected by
prevailing rhizospheric salinity (Egamberdiyeva and Islam 2008). Diverse plant–
microbe interactions in rhizosphere soil greatly differ from species to species and
also differ from those occurring in the surrounding soil. Because of rich nutrient
availability, the rhizosphere is an appropriate survival niche for soil
microorganisms (Ahmad et al. 2008). Studies on the genetics and morphology of
rhizobacterial species have further clarified the communication mechanisms that
function between the host root system and microorganisms (Tripathi et al. 2002).
In lands that are greatly degraded by salinity, the microbial community is greatly
influenced. However, halotolerant bacteria seem to grow abundantly in soils with
a salt concentration of up to 30% and in lands that are
devoid of salt (Khan et al. 2016). Therefore, they can thrive in rhizosphere soil of
various halophytic species with a low water potential (Ruppel et al. 2013). More
astonishingly, the plant growth–promoting properties of various PGPRs isolated
from halophytic rhizospheres are maintained under high salinity. The salt-tolerant
PGPR Kushneria species YCWA18, isolated from the eastern coast of China, has
demonstrated optimal growth even in a salt solution containing 20% NaCl (Zhu et
al. 2011). Various other PGPRs that have been isolated have salt-tolerant
characteristics, shown by their growth in NaCl concentrations of up to 25%. These
include Arthrobacter, Halomonas, P. mendocina, Bacillus pumilus, and
Nitrinicola lacisaponensis. Along with maintenance of growth, these species have
other growth- promoting features such as efficient phosphorus solubilization and
production of indoleacetic acid (IAA), siderophores, and 1-aminocyclopropane-1-
carboxylate (ACC) deaminase (Tiwari et al. 2011). A plant growth–promoting
(PGP) trait is defined as the capability to provide P to the host in a P-limited
environment. This phytohormone-like feature of PGPRs stimulates plant growth,
providing sufficient Fe to the host and reducing the level of ACC deaminase, a
precursor of ethylene production (Etesami and Beattie 2018). From earlier reports
it is known that the nodules of leguminous species are more salt sensitive than the
rhizobacteria present in the rhizosphere of legumes. Isolation of bacterial species
from leguminous rhizospheres mainly include Bacillus spp., which are Gram-
positive bacteria. Among rhizospheric PGPRs, Pseudomonas spp. in the
rhizosphere of rice is most common (Rangarajan et al. 2002). These
species includes P. fluorescens,
P. pseudoalcaligenes, and P. diminuta. Fluorescent pseudomonads, P. alcaligenes,
and P. pseudoalcaligenes have been found in both saline and nonsaline conditions.
However, these species, isolated from the wild rice S. salitolerans, were capable
of nitrogen fixation and increased P solubilization under salinity. Nonetheless,
there is a lack of a definitive taxonomic categorization of PGPRs growing in saline
soil (Loganathan and Nair 2004). Besides wide dominance of Pseudomonas and
Flavobacterium spp. over Arthrobacter and Bacillus spp., Bacillus spp. are wide-
spread in a variety of natural habitats. However, Azotobacter spp. have been
isolated mostly from salt-affected areas. This suggests a diverse habitat range and
efficient adaptability of Bacillus. Apart from the wild rice variety, various salt-
tolerant bacteria have also been isolated from Salicornia brachiata. These include
Haererehalobacter, Zhihengliuella, Rhizobium radiobacter, and Brachybacterium
saurashtrense. These species were reported to have plant growth–promoting
effects on S. brachiata, such as enhanced P solubilization, IAA production, and
ACC deaminase synthesis under salinity (Jha et al. 2012). Apart from bacteria
isolated in India, Zhihengliuella isolated from northwest China can withstand
NaCl concentrations of up to 25% (Zhang et al. 2007). The rhizosphere of rice is
reported to colonize various N2-fixing endophytic diazotrophs such as
Pseudomonas spp. (Jha et al. 2009). In addition, from the endorhizosphere of
Salicornia europea,
P. pseudoalcaligenes has been isolated (Ozawa et al. 2007). Of the rhizospheric
bacteria that were isolated from the halophyte Aster tripolium, 36% were
firmicutes, 9% were proteobacteria, and 55% were actinobacteria (Szymańska et
al. 2016). The diversity of bacterial species in the roots of A. tripolium is limited
to Gram-positive
bacteria. Growth of Gram-positive bacteria in salt-dominated areas has previously

been reported (Damodaran et al. 2013). There are primarily three genera of
bacteria that dominate the rhizosphere soil of plants: Streptomyces, Bacillus, and
Pseudomo- nas (Bouizgarne 2013). Herbaspirillum, Azospirillum, P. alcaligenes,
Gluconacetobacter, Serratia, and many other species have also been identified in
rhizosphere soil (Szymańska et al. 2016). Signature lipid biomarker (SLB)
analysis is of great importance for characterizing diversity in the structure and
function of rhizospheric microorganisms (Mrozik et al. 2014). PGPR strains
isolated from Suaeda fruticosa, which show optimum growth even under a 300-
mM NaCl concentration, showed potential PGP characteristics, and their traits
were screened under high salinity (Goswami et al. 2014). Isolation of rhizospheric
bacteria from the medicinal plant Ajuga bracteosa has also been reported (Kumar
et al. 2012). The PGP trait is often altered by biosynthesis of chitinase, ion-
chelating siderophores, and microbial antagonists (such as hydrogen cyanide
(HCN)), and, as a result, the growth of the plant is affected (Zhou et al. 2012b).
PGPRs such as Bacillus have been isolated from the rhizosphere soil of various
halophytes such as Atriplex leucoclada, Salicornia virginica, Haloxylon
salicornicum, and Arthrobacter pascens (Ullah and Asghari 2015). The
rhizospheres of various halophytes have been reported to colonize a variety of salt-
tolerant PGPR species. These halophytic species include Salicornia bigelovii
(Rueda-Puente et al. 2010), Halocnemum strobilaceum (Al-Mailem et al. 2010), S.
brachiata (Jha et al. 2012), Sesuvium portulacastrum (Bian et al. 2011; Anburaj et
al. 2012), and Acacia spp. (Boukhatem et al. 2012). Apart from the diversity of the
halophytic rhizospheres in which these PGPRs were found, they were also isolated
from diverse habitats ranging from saline to alkali–saline and desert soils.
4.6 Growth-Stimulating Mechanisms of PGPRs Under

Stress Conditions
The mechanisms by which PGPRs enhance the growth of plants mainly include
growth hormone biosynthesis and improved uptake and mobilization of nutrients
from soil to plant parts. Apart from these, PGPR-induced tolerance of salinity
greatly influences the survival of plants under harsh saline conditions (Glick 2010;
Sandhya et al. 2010a; Ma et al. 2011). However, different free-living soil bacteria
belonging to particular genera may have different degrees of influence on plant
growth. To alleviate stress effects on plants, rhizobacterial species can be used in
different ways. PGPRs have multidimensional effects on plant growth, both direct
and indirect. The indirect methods include protection from negative effects of
plant pathogens through secretion of antipathogenic substances (Nadeem et al.
2013). The growth-promoting feature of PGPRs is implemented by synthesis of
various secondary metabolites with significance potential for growth promotion or
enhancement of nutrient uptake by plants. In addition, they enhance the growth of
the host plant by enhancing nitrogen fixation and increasing the availability of P to
the plants.
Fig. 4.1 Cellular mechanisms involved in alleviation of salt stress through interaction of plant
growth–promoting rhizobacteria (PGPRs) and plants. Increases in the activity of ion transporters
maintain the osmotic balance and minimize osmotic damage. Bacterial secretions such as
exopolysaccharides increase cation exchange and water retention; polyamines increase the levels
of storage protein and antioxidant activity; bacteriocins are responsible for alterations in stress-
related proteins and lipo-chitooligosaccharides which increases nodulation by increasing the
activity of Nod factors. An up arrow represents an increase in activity; a down arrow represents
a decrease in activity
The halophytic rhizosphere contains a diverse ecological colonization of

microorganisms that are salt tolerant and induce plant growth. PGPRs adopt
several mechanisms to enhance growth in plants and protect them from various
environmental stresses such as salinity and drought. The cellular mechanisms of
PGPR– plant interactions in ameliorating the salinity effect are depicted in Fig.
4.1. These mechanisms include synthesis of ACC deaminase, enhancement of
biological nitrogen fixation, phytohormone production, and exopolysaccharide
synthesis. The abilities of PGPRs to enhance plant growth in both conventional
and extreme habitats, and to facilitate plant adaptation to extreme environments,
have been studied (Hayat et al. 2010). Rhizospheric bacteria promote plant growth
in direct and indirect ways. The direct mechanisms include better nutrient fixation
and solubilization, as well as enhanced phytohormone synthesis. An indirect
mechanism is minimization of the deleterious effects of phytopathogens through
biocontrol of their growth on the host plant (Mapelli et al. 2013). Among the
different environmental stresses, salinity has the most deleterious effects on plant
growth and crop yields (Mayak et al. 2004). Halophytic species are dominant in
the dry regions of the world. Halophytes have their own ability to reclaim
agricultural soil affected by high salinity (Ravindran et al. 2007). A number of
works have lately enriched the existing understanding of host–microbe
interactions and the beneficial roles of rhizospheric microbes in enhancing plant
resistance to various abiotic stresses. These studies have
Fig. 4.2 Salt tolerance mechanisms of halotolerant plant growth–promoting rhizobacteria

(PGPRs) and beneficial effects of PGPR inoculation in ameliorating detrimental effects of
salinity
delivered substantial knowledge about (1) plant–microbe interactions,

(2) mechanisms of plant growth under saline conditions, and (3) potential bacterial
strains that can be used as biofertilizers in saline lands (Mapelli et al. 2013). The
effects of salinity on glycophytes and the mechanisms of PGPR-mediated salt
tolerance are depicted in Fig. 4.2. This type of tolerance that is provided by
PGPRs is termed systemic tolerance (Yang et al. 2009). PGPRs that induce plant
growth fall into three categories: biofertilizers, phytostimulators, and
biopesticides. Biofertilizers enhance the availability of N and P to the host,
phytostimulators induce biosynthesis of phytohormones, and biopesticides reduce
the risks of pathogen attacks on the host. Various studies have illustrated the
beneficial role of PGPRs in alleviating stress effects on various crop species (Ali
et al. 2009; Kohler et al. 2009; Sandhya et al. 2010a). Enhanced growth through
PGPR inoculation is achieved by extensive root formation stimulated by increased
production of phytohormones (such as IAA and nitric acid) and increased
biosynthesis of ACC deaminase (Dimkpa et al. 2009).
4.6.1 Growth Promotion by Enhanced ACC Deaminase Activity
Elevated biosynthesis of ACC deaminase reduces ethylene production, which

confers tolerance to different environmental stresses (Lucy et al. 2004; Bal et al.
2013). Many reports have described the beneficial influence of PGPRs on growth
in terms of enhanced ACC deaminase activity and improvement of salinity
tolerance in host plants (Table 4.1). Ethylene, a plant stress hormone, is released as
a stress response upon encounters with various environmental stresses. Salinity
causes
Table 4.1 Plant growth–promoting rhizobacteria (PGPRs) with 1-aminocyclopropane-1-carbox-

ylate (ACC) deaminase activity implemented for improvement of salt tolerance capabilities in
various glycophytic crop species
Plant species PGPRs Effects on plants References
Brassica Methylobacterium Promoted root elongation Madhaiyan
campestris fujisawaense et al. (2006)
Brassica Brevibacterium Increased root length and dry Siddikee et al.
campestris epidermidis RS15 biomass accumulation (2010)
Brassica Bacillus circulans, Increased root and shoot Ghosh et al.
campestris Bacillus firmus, Bacillus length; increased fresh and dry (2003)
globisporus biomass
Dianthus Azospirillum brasilense Inoculated cuttings produced Li et al. (2005)
caryophyllus the longest roots
Pisum Rhizobium Enhanced nodulation in plants Ma et al. (2003)
sativum leguminosarum
Zea mays Enterobacter sakazakii Increased agronomic Babalola et al.
parameters (2003)
Zea mays Pseudomonas Root elongation Shaharoona
et al. (2006)
Zea mays Pseudomonas syringae, High relative water; high Nadeem et al.
Enterobacter chlorophyll; low proline (2007)
aerogenes, content
Pseudomonas
fluorescens
Oryza sativa Variovorax, Increased root and shoot Bal et al. (2013)
Rhodococcus length; increased root fresh
biomass
Oryza sativa Enterobacter Increased growth parameters Sarkar et al.
and activities of various (2017)
antioxidant enzymes
Lycopersicon Pseudomonas Increased root biomass Belimov et al.
esculentum brassicacearum (2007)
Lycopersicon Bacillus pumilus, Increased vigor index under Damodaran
esculentum Bacillus subtilis saline–sodic conditions et al. (2013)
Lycopersicon Achromobacter Improved rate of Mayak et al.
esculentum photosynthesis (in comparison (2004)
with noninoculated plants)
under saline conditions
Lactuca Azospirillum Better germination and Barassi et al.
sativa vegetative growth under (2006)
salinity
Arachis Pseudomonas Greater growth (in comparison Saravanakumar
hypogaea fluorescens with noninoculated plants) and
under saline conditions Samiyappan
(2007)
Triticum Pseudomonas, Serratia Improved shoot and root Zahir et al.
aestivum growth and growth- (2009)
contributing parameters
(continued)

Plant species PGPRs Effects on plants References
Avena sativa Klebsiella Increased growth parameters; Sapre et al.
lower levels of various stress (2018)
indicators such as MDA and
proline
Avena sativa Acinetobacter Increased growth parameters Xun et al.
and antioxidant enzyme (2015)
activity
various physiological changes in plant tissues by means of overproduction of

ethylene through increased synthesis of ACC (Tank and Saraf 2010). PGPRs
facilitate plant growth through enhanced biosynthesis of ACC deaminase under
various abiotic stress conditions. Earlier studies described plant growth promotion
under various abiotic stresses and pathogen attack, with PGPRs reducing the
ethylene level through enhanced ACC deaminase activity. Numerous species of
Gram-negative bacteria (Wang et al. 2000; Babalola et al. 2003), Gram-positive
bacteria (Ghosh et al. 2003; Belimov et al. 2007), and rhizobia (Ma et al. 2003;
Uchiumi et al. 2004) have been reported to show ACC deaminase activity. The
PGP capabilities of numerous microbial species—such as Methylobacterium
fujisawaense, Burkholderia, Ralstonia solanacearum, Enterobacter,
Agrobacterium genomovars, and Rhizobium—have been studied (Hontzeas et al.
2004; Pandey et al. 2005; Blaha et al. 2006). ACC deaminase induces plant
growth via reduced biosynthesis of ethylene through conversion of this ethylene
precursor (ACC) to α-ketobutyrate and ammonia (Saleem et al. 2007). Further
reduction of ethylene biosynthesis can be achieved by ACC deaminase competing
with ACC oxidase, which has more affinity for ACC, resulting in lower
endogenous synthesis of plant ethylene (Saleem et al. 2007). To achieve this, the
level of ACC deaminase in the plant must be a minimum of 100 times higher than
the level of ACC oxidase. Biosynthesis of IAA was occurred from the tryptophan
and secreted by PGPR and get adsorbed by the plants. The newly produced IAA is
added to the existing endogenous IAA pool and induces growth. Apart from this,
IAA facilitates conversion of S-adenosylmethionine (SAM) into ACC by
stimulating ACC synthetase activity (Saleem et al. 2007). The ACC deaminase
activity of rhizobial microorganisms can stimulate ACC production and exudation
from plant roots, which provides a unique nitrogen source to the microorganisms
to stimulate root growth. Alterations in the ACC deaminase activity of various
microorganisms under environmental stresses play a positive role in
phytoremediation. The ACC deaminase activity of rhizobacteria induces growth of
plants and mediates rhizodegradation through root exudates, biotransforming nox-
ious elements. Apart from this, phytoremediation of heavy metals is achieved
through the presence of rhizobacteria in the rhizosphere soil of various halophytes
(Singh and Jha 2016; Singh et al. 2015). Rhizobacteria producing ACC deaminase
enhance plant growth by implementation of different strategies such as alleviation
of detrimental effects of various environmental stresses, delayed senescence,
protection
against phytopathogens, and induction of nodulation in legumes (Ali et al. 2012).

PGPRs that inhabit saline environments and show ACC deaminase activity have
been isolated and used for alleviation of negative effects of salinity on the growth
of various crop plants. For example, the growth of maize shoots and roots was
enhanced by 2.3-fold and 3.3-fold upon inoculation with P. fluorescens N3 and
P. putida (PGPRs with ACC deaminase activity), respectively, in comparison with
controls (Khan et al. 2016). Similarly, enhanced nodule formation in leguminous
crops inoculated with ACC deaminase–producing rhizobacteria was also reported
(Shaharoona et al. 2006). Moreover, it has been documented in wheat plants that
the PGPR strain Azospirillum brasilense FP2 reduces ACC oxidase activity
(Camilios- Neto et al. 2014). In addition, higher activity of ACC deaminase was
reported in the PGPR strain Pseudomonas maricaloris, isolated from Avicennia
marina (El-Tarabily and Youssef 2010). Upon inoculation with these strains,
seedlings exhibited decreased level of ACC and higher growth rates under salinity
stress (El-Tarabily and Youssef 2010). Reductions of 44%, 53%, and 57% in
ethylene levels were observed in pepper plants after inoculation with
Zhihengliuella alba, Brevibacterium iodinum, and Bacillus licheniformis (isolated
from halophytes), respectively.
4.6.2 Growth Promotion by Enhanced Endogenous Phytohormone

Production
Phytohormones are essential in regulating the stress responses of plants to various

environmental stresses, and in maintaining normal plant physiology and
conferring tolerance of salinity and other environmental stresses (Ryu and Cho
2015). The responses of plants to salinity induce a variety of alterations in
molecular, biochemical, and physiological aspects. The responses vary according
to the frequency and intensity of the salinity, the environmental conditions, the
physical and chemical properties of the soil, and the age of the plants (Kumari et
al. 2015). Application of exogenous phytohormones can be useful for amelioration
of the adverse effect of salinity (Zahir et al. 2010). The hormonal status of plants
is modulated by soil bacteria, which release exogenous phytohormones that
contribute to enhanced salinity tolerance (Ilangumaran and Smith 2017).
Exogenous phytohormones can alter the levels of endogenous phytohormones,
providing a way to counter salt stress conditions (Ilangumaran and Smith 2017).
Modulation of the plant hormonal balance is one of the strategies that PGPRs
adapt to enhance plant growth (Tsukanova et al. 2017). Among phytohormones,
most of the salt-tolerant PGPRs induce biosynthesis of IAA and, as a result,
improve the growth of salinity-treated seedlings (Tiwari et al. 2011). PGPRs may
also alter root-to-shoot hormonal signaling, improving crop salt tolerance (Yang et
al. 2009). Higher production of IAA in plants, induced by salt-tolerant
rhizobacteria, was shown to be responsible for increased root growth in coastal
soils (Siddikee et al. 2011). The species from the roots of which the PGPRs were
isolated included Argentina and Prosopis strombulifera (Sgroy et al. 2009; Tiwari
et al. 2011; Piccoli et al. 2011; Bian et al.
2011). Salinity-induced levels of abscisic acid (ABA) were counteracted by the

Bacillus amyloliquefaciens strain SQR9, which improved salt stress tolerance in
maize by increasing chlorophyll and total soluble sugar content, with increased
activity of various antioxidant enzyme components (Chen et al. 2016). Bacterial
cytokinins can also be responsible for salt tolerance, but fewer studies have
reported this. PGPR strains enhanced growth by 52% and alleviated salinity-
induced dor- mancy in wheat (Egamberdieva 2009). Improvements in lettuce
seedling growth under water stress conditions by cytokinin-producing Bacillus
subtilis were reported by Arkhipova et al. (2007). Synthesis of excess ethylene is
regulated by PGPRs producing ACC deaminase (Glick et al. 2007). Inoculation of
Solanum lycopersicum with P. putida UW4 increased the shoot biomass under
saline conditions (Yan et al. 2014). IAA accumulation on plants induces the
activity of the ACC synthase gene, resulting in greater accumulation of ACC.
Higher concentrations of ACC lead to greater production of ethylene. PGPRs with
ACC deaminase activity reduce accumulation of ACC by breaking down excess
ACC, which, in turn, reduces ethylene production under various environmental
stresses. Several studies have documented the role of bacterial ABA in influencing
the ABA status of plants. Modulation of the ABA signaling cascade of wheat has
been reported upon inoculation with halotolerant Dietzia natronolimnaea STR1
via upregulation of different ABA-responsive genes (Bharti et al. 2016). Similarly,
the ABA-producing bacterial strains Burkholderia cepacia SE4 and
Promicromonospora sp. SE188 enhanced shoot biomass accumulation in Cucumis
sativus under saline conditions (Kang et al. 2014). Cotton seedlings inoculated
with P. putida Rs-198 had a lower ABA content and increased biomass
accumulation under salt stress (Yao et al. 2010). Arthrobacter protophormiae
SA3–inoculated wheat showed greater salinity tolerance, with increased levels of
IAA and less accumulation of ABA and ACC.
4.6.3 Enhancement of Micronutrient Availability to Plants by

Siderophore-Producing PGPRs
Siderophores are Fe-chelating compounds and have high affinity for iron.
Siderophores make iron more accessible to plants by formation of an Fe-
siderophore complex. In saline and sodic soils the level of iron available for
uptake by plants is limited. The low availability of iron and other micronutrients
needed by the plants in this type of soil results in iron deficiency (Abbas et al.
2015). The siderophore production ability of PGPRs increases the availability of
micronutrients to plants (Navarro-Torre et al. 2017; Zhou et al. 2017). Bacterial
siderophores are used by plants as an iron source. In addition, the bacterial
siderophores prevent the spread of harmful microorganisms and their deleterious
effects on plant growth (Shailendra Singh 2015). Earlier reports described the
ability of PGPRs to synthesize siderophores (Kuffner et al. 2008). Along with
auxin production, plant growth in metal-polluted soil is supported by
siderophore-
producing soil and rhizospheric bacteria. Bacterial stains such as Pseudomonas

sp. BE3dil, Janthinobacterium lividum, S. marcescens, and Flavobacterium
frigidimaris have been reported to have the ability to produce siderophores
(Kuffner et al. 2008). Previous reports have suggested that plant growth can be
enhanced by siderophore-producing PGPRs (Glick 2003).
4.7 Implementation of PGPRs in Development of Salt-

Tolerant Crop Species
Growth improvements in crops grown in saline conditions by use of different salt-

tolerant PGPRs have been reported in several studies (Mayak et al. 2004; Shukla
et al. 2012; Qin et al. 2016) (Table 4.2). In the modern era, various environmental
factors such as salinity have caused reductions in agricultural productivity in
developing countries (Shukla et al. 2012). Salinity alters many basic
physiological processes of plants, affecting their yields. Various factors exert
different negative effects on growth and cause growth reductions in plants grown
under high salinity— most importantly, imbalances between nutrient uptake and
distribution. These further generate competitions between essential
macronutrients such as K+, Ca2+, and NO3—, and prevailing Na+ and Cl—. To
counter this, implementation of PGPR-based salinity tolerance to boost beneficial
mechanisms in various agricultural crops is a revolutionary technique being used
alongside traditional methods (Jha et al. 2012). As discussed earlier, several
mechanisms are employed by halotolerant PGPRs to improve plant growth, such
as (1) efficient regulation of antioxidant defenses for scavenging of ROS (Jha and
Subramanian 2014; Qin et al. 2016); (2) improved fixation of atmospheric
nitrogen, resulting in improved nutrition supply to the plants, better P
solubilization, and increased production of siderophores; (3) restriction of toxic
Na+ and Cl— within the tolerance limits of plants by selective absorption of ions
and maintenance of a high K+-to-Na+ ratio (Shukla et al. 2012; Etesami 2018); and
(4) secretion of extracellular polymeric substances (EPSs) forming a physical
barrier, called a rhizosheath, which reduces Na+ uptake by the roots and
translocation to the shoots. Halotolerant PGPRs improve the soil structure by
producing EPSs. These promote aggregation of the soil, which, in turn, increases
the water retention capacity of the soil and increases nutrient availability to the
plants. A functional characteristic of bacteria is that they contain functional groups
such as hydroxyl, sulfhydryl, carboxyl, and phosphoryl groups, which bind to Na +
and reduce its uptake and translocation (Nunkaew et al. 2014). Various
halotolerant bacteria such as Halomonas variabilis, Enterobacter, Paenibacillus,
Planococcus rifietoensis, and Aeromonas hydrophila/caviae produce EPSs and
induce biofilm synthesis (Qurashi and Sabri 2012; Khan et al. 2016). Various
studies have described the important role of PGPRs in alleviating salt stress in a
variety of crops such as groundnut, rice, tomato, and red pepper (Shukla et al.
2012; Bal et al. 2013; Upadhyay and Singh 2015). In groundnut grown under high
salinity, increased levels of chlorophyll, proline, and malondialdehyde, along
with other physiological parameters, were
Table 4.2 Interaction of plant growth–promoting rhizobacteria (PGPRs) with various crop
species and responses of the host plants
Halophytic
rhizosphere
from which
PGPRs were Plant response to
Crop PGPR strain isolated PGPRs References
Solanum Achromobacter Lycium shawii Increased fresh weight, Mayak et al.
lycopersicum piechaudii dry weight, and water (2004)
ARV8 use efficiency of tomato
through decreased
ethylene production
under stress
Solanum Azotobacter, Halophyte Increased IAA, Damodaran
lycopersicum Bacillus grasses siderophores, and et al. (2013)
safensis, phosphate
Bacillus solubilization
subtilis,
Rhizobium
Zea mays Bacillus Haloxylon Increased growth Ullah and
pumilus, salicornicum, parameters; higher Asghari
Arthrobacter Lespedeza chlorophyll and sugar (2015)
aurescens, bicolor, content; increased
Arthrobacter Salicornia activity of antioxidant
pascens virginica enzymes such as CAT
and SOD
Eggplant Bacillus subtilis – Increased plant auxin Bochow
synthesis with et al. (2001)
changing regulation of
the appropriate
mechanisms induced
by bacterial production
of auxin and auxin
precursors during root
colonization
Vigna Pseudomonas Salt-affected Increased growth Ahmad
radiata syringae, Vigna radiata parameters such as et al. (2012)
Pseudomonas shoot and root fresh
fluorescens weight; improved water
use efficiency
Triticum Bacillus Salt-affected Improved growth Ashraf et al.
aestivum insolitus, wheat parameters in (2004)
Aeromonas inoculated samples
hydrophila (in comparison with
uninoculated samples);
higher Ca2+ levels in
inoculated samples
contributed to lower
Na+ uptake
(continued)

Halophytic
rhizosphere
from which
PGPRs were Plant response to
Crop PGPR strain isolated PGPRs References
Triticum Bacillus Saline area of Inoculated samples Upadhyay
aestivum subtilis, the eastern showed lower activity et al. (2012)
Arthrobacter Gangetic Plain of antioxidant enzymes
such as APX, CAT, and
GR, suggesting lower
ROS production
Raphanus Staphylococcus Plants naturally Bacterial treatments Hayat et al.
sativus kloosii, Kocuria grown on high under salinity (2010)
erythromyxa salty soils in the conditions had positive
upper Çoruh effects on plant growth,
Valley with increased
chlorophyll content
Capsicum Brevibacterium West coast soil Enhancement of growth Siddikee
annuum iodinum, of the Yellow and salt tolerance by et al. (2011)
Bacillus Sea regulation of stress
licheniformis ethylene synthesis
Oats Acinetobacter, Salt-tolerant Enhancement of Sapre et al.
Klebsiella wheat growth; less electrolyte (2018)
leakage; lower MDA
levels
Oryza sativa Enterobacter Salt-tolerant rice Increased phosphate Kim et al.
solubilization, IAA (2014)
production, and
siderosphere
production
APX ascorbate peroxidase, CAT catalase, GR glutathione reductase, IAA indoleacetic acid,
MDA malondialdehyde, ROS reactive oxygen species, SOD superoxide dismutase
reported in response to inoculation with beneficial PGPRs (Shukla et al. 2012).

Improved salt tolerance of oat plants inoculated with halotolerant PGPRs such as
Acinetobacter has also been reported (Xun et al. 2015). In salinity tolerance
studies of barley (Chang et al. 2014) and oats (Sapre et al. 2018), plants inoculated
with various PGPRs showed higher tolerance of salinity than uninoculated control
plants. The salinity tolerance of rice has been improved by inoculation with a
halotolerant Enterobacter PGPR, which alleviated the negative effects of salinity
and improved the growth of the plants (Sarkar et al. 2017). Increases in the
germination rate, the seedling growth rate, the length and biomass of shoots and
roots, and chlorophyll levels have been reported in rice inoculated with an
Enterobacter PGPR. The enhanced growth of the plants inoculated with
Enterobacter strain P23 may have been attributable to its PGP traits. Reduced
activity of various antioxidant enzymes
along with proficient growth of rice under saline conditions suggest that ROS
generation is reduced upon inoculation with PGPRs (Sarkar et al. 2017). Similar
findings have been documented in lettuce inoculated with Rhizobium sp. and
Serratia sp. (Lee et al. 2005), in wheat inoculated with Arthrobacter sp. and
B. subtilis (Upadhyay et al. 2012), and in rice inoculated with B. pumilus and
P. pseudoalcaligenes (Jha and Subramanian 2014) under saline conditions. In
addition to limiting ROS production, PGPRs increase biosynthesis of IAA, which,
in turn, induces plant growth and, most importantly, root growth. Achievement of
salinity tolerance in tomato through inoculation of the plants with Enterobacter
sp. EJ01 was demonstrated by Kim et al. (2014). The salinity tolerance may have
been attributable to transcriptional activation of various stress-responsive factors
prior to the induction of salinity (Kim et al. 2014).
4.8 Conclusion and Future Perspectives
PGPRs isolated from a saline rhizosphere are able to mitigate the deleterious
impacts of salinity and increase germination as well as the viability index, shoot
and root length, dry biomass production, and, most importantly, the agricultural
yield. PGPRs are used in organic farming practice as biofertilizers and biocontrol
agents. Explora- tion of soil microbe diversity is essential to meet global food
demands despite increasing deterioration of soil quality caused by increases in the
prevalence and severity of salinity, which affect agricultural productivity. Plants
have developed efficient strategies to enhance their tolerance of abiotic stresses
such as high salinity and drought. PGPRs associated with the halophytic
rhizosphere can mitigate the negative effects of prevailing salinity in a cost-
effective manner where there is an urgent need for salt-tolerant crop varieties.
Therefore, inoculation of agricultural crops with salt-tolerant PGPRs is an efficient
strategy for sustainable agriculture in salt-affected areas. Research on PGPRs must
be carried out to open up new avenues of opportunity to develop salinity-tolerant
agricultural crops. Research is now being carried out to deepen our fundamental
knowledge of microbe–halophyte interactions and to take that knowledge to
another level for production of salt-tolerant crop varieties. Unraveling the
molecular mechanisms of salt tolerance of PGPRs will allow us to engineer
bacteria with enhanced ability to stimulate plant growth under saline conditions.
Furthermore, the efficiency of PGPRs for stimulation of plant growth under
salinity must be assessed over longer periods of time for relevant crop production.
Apart from being useful for production of salt-tolerant crop varieties, PGPRs can
be implemented in phytodesalinization of salt-affected agricultural lands,
phytoremediation, and biological control of various types of pathogen attack.
Strategies for rapid identification of efficient PGPR strains to be used as
bioinoculants must be developed to improve growth of crops under saline
conditions. With increasing exposure of agricultural lands to various
environmental stresses, it is now essential to develop salt-tolerant crop varieties,
and utilization of stress-tolerant PGPRs is paving the way toward fulfilling this
goal.
Acknowledgements A.K.P. received a grant from the Science and Engineering Research Board
(SERB) (grant number SB/SO/PS-14/2014), Department of Science and Technology (DST),
Government of India (New Delhi, India), which is duly acknowledged. This manuscript has been
assigned the Council of Scientific and Industrial Research–Central Salt and Marine Chemicals
Research Institute (CSIR-CSMCRI) registration number PRIS 074/2018.
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615032
Halotolerant Plant Growth-Promoting
Fungi and Bacteria as an Alternative 5
Strategy for Improving Nutrient Availability
to Salinity-Stressed Crop Plants
Hassan Etesami and Hossein Ali Alikhani
Abstract
Nowadays, it is imperative to address the management of crop production in
difficult environmental conditions in order to achieve the maximum potential of
plant growth and yield for providing enough food. Increasing demand for plant
products has been coupled with decreasing cultivated land due to the limitation
of water and soil resources. Salinity is one of the most important abiotic
stresses that both limit the production of agricultural products in arid and
semiarid areas and decrease arable land across the world. Plant nutrition
imbalances due to excessive absorption of sodium (Na+), and chloride (Cl—)
ions also reduce the absorption of macronutrients such as potassium (K),
calcium (Ca), magnesium (Mg), nitrogen (N), and phosphorus (P) and
micronutrients such as iron (Fe), zinc (Zn), copper (Cu), manganese (Mn), and
boron (B). To satisfy crop nutritional requirements under salinity stress, micro-
and macronutrients are usually added to soil as chemical fertilizers; however
synthesis of these fertilizers is highly energy- intensive processes and has long-
term impacts on the environment in terms of eutrophication, soil fertility
depletion, and carbon footprint. Such environmental concerns have led to the
search for sustainable way of providing crops with nutrients. In this regard,
plant growth-promoting salinity-tolerant microorganisms have been seen as
best eco-friendly means for nutrition of salinity-stressed crop plants. These
microorganisms increase the nutrient bioavailability through N 2 fixation and
mobilization of key nutrients (P, K, and micronutrients) to the crop plants. Use
of salinity-tolerant microorganisms is also known as an alternative, innovative,
environmental friendly option to reduce the use of costly and
H. Etesami (*) · H. A. Alikhani

Department of Soil Science, University College of Agriculture and Natural Resources,
University of Tehran, Tehran, Iran
# Springer Nature Singapore Pte Ltd. 2019

103
104 H. Etesami and H. A. Alikhani
non-environmental friendly chemical fertilizers and can represent a promising

approach to increase nutrient bioavailability and facilitate the development of
saline soil-based agriculture. In this chapter, current knowledge on the
mechanisms used by plant growth-promoting rhizobacteria (PGPR) and
arbuscular mycorrhizal (AM) fungi to influence soil nutrient bioavailability
(N, P, K, and micronutrients) under salinity stress is discussed.
Keywords
Arbuscular mycorrhizal fungi · PGPR · Salinity stresses · Agriculture crops ·
Plant-microbe interactions · Saline soil-based agriculture
5.1 Introduction
Given the growing population of the world with an annual growth rate of 80
million per year and the food shortage crisis of the present century, it is necessary
to look for a proper way to meet the food needs of the community in an adequate
and desirable quality because one of the indicators of sustainable development is
the issue of food security. In order to meet the food needs, given the declining
trend in agricultural land that is mostly due to soil salinization, there is no solution
other than the strategy of increasing production per unit area (maximum
production) (Etesami and Beattie 2018). Due to the ever-increasing demand for
food and the lack of salt non-affected soils, we should inevitably use the potential
of salinity-stressed soils to produce important crop plants. Salinity of water and
soil is among the most important factors limiting the growth of crop plants and
production of agricultural products. The total area affected by salt in the world is
constantly rising. According to the estimates, around 30–50% of the world’s land
is under salt stress, and in Iran, about 50% of the cultivated land is facing a
salinity problem. In saline conditions, sodium ion (Na +) concentration is usually
higher than the concentration of micro- and macronutrients, and this leads to
nutritional imbalances in plants under salt stress in a variety of ways. In general,
the presence of excess salts in soil or irrigation water confronts the plant with salt
stress. Salinity stress, irrespective of the mechanism of salinization, occurs due to
excessive accumulation of cations and anions in the soil solution. These salts
consist primarily of ions such as Na+ and chlorine (Cl—) and then bicarbonate
(HCO3—), sulfate (SO42—), calcium (Ca2+), magnesium (Mg2+), borate (BO3—3), and
rarely nitrate (NO3—) (Sha Valli Khan et al. 2014). The presence of these cations
and anions in the soil prevents the absorption of other essential nutrients such as
nitrogen (N), phosphorus (P), potassium (K), iron (Fe), cupper (Cu), zinc (Zn),
etc. (Giri et al. 2007; Munns and Tester 2008; Tester and Davenport 2003). To
increase the availability of nutrients for salinity-stressed plants, large amounts of
chemical fertilizers are required on a regular basis. In areas where there is a
problem of water and soil salinity, salinity causes a 10–60% reduction in the yield
of crops (FAO 2005). In these areas, farmers are trying to compensate for the
damage caused by salinity by using more inputs such as fertilizer, seeds, and
water, which sometimes accounts for up to 65% of the income of the farmers. But,
in
5 Halotolerant Plant Growth-Promoting Fungi and Bacteria as an Alternative.. . 105
addition to increasing production costs, the excessive use of these fertilizers

causes a lot of environmental problems including increasing pollution of water and
soil resources (greenhouse gaseous emissions) as well as water eutrophication,
imbalance of nutrients in the soil, decrease in the yield of agricultural products,
and endangering the health of humans and other living organisms (Adesemoye and
Kloepper 2009). Moreover, the use of chemical fertilizers in salt-affected soils is
not a right choice and, if used, increases the salinity of the soil. Most crop plants
are sensitive to salinity and cannot survive under high salinity concentrations
(Siddiqui et al. 2009). In other words, such plants need microorganisms to grow in
saline soils (Etesami and Beattie 2018). For this reason, in recent years, the use of
plant growth- promoting microorganisms (PGPMs) as bio-fertilizers or biocontrol
agents in agriculture has been considered by many researchers, and the increased
growth of different crops by these microorganisms has been proven in greenhouse
and field experiments. Use of PGPMs is known as an alternative, innovative,
environmental friendly option to reduce the use of costly and non-environmental
friendly chemical fertilizers (Rashid et al. 2016). PGPMs increase plant growth
and yield through various mechanisms (Etesami and Maheshwari 2018).
Rhizosphere free living bacteria that directly and indirectly improve plant
growth and health are named as plant growth-promoting rhizobacteria (PGPR). In
indirect mechanisms, the PGPR indirectly modify the harmful effects of plant
pathogens by using specific mechanisms, thereby increasing plant growth. But in
direct mechanisms, these bacteria, by fixing nitrogen, producing the metabolites
effective at plant growth, such as plant hormones indole-3-acetic acid (IAA),
cytokinins (CK), and gibberellins (GAs), increasing the solubilization of insoluble
compounds such as P and K through the production of organic and inorganic
acids, producing siderophores (increase in the availability of micronutrients such
as Fe, Zn, etc.), and reducing the effects of stress ethylene by the production of
enzyme ACC (1-aminocyclopropane-1-carboxylate) deaminase, help plants to
grow more efficiently (Etesami 2018; Etesami and Maheshwari 2018; Gamalero
and Glick 2011; Glick 2014). Various genera of bacteria such as Pseudomonas,
Azospirillum, Azoto- bacter, Klebsiella, Enterobacter, Alcaligenes, Arthrobacter,
Burkholderia, Bacillus, Serratia, Erwinia, Flavobacterium, and Rhizobium have
been reported as PGPR (Egamberdiyeva 2005; Glick 2014).
Another group of microorganisms that are closely associated with plants are
fungi. Fungi, like bacteria, can colonize the rhizosphere, the rhizoplane, and in
many cases within root tissues (endophyte). Arbuscular mycorrhizal (AM) fungi
are among the most abundant fungi in agricultural soils. Mycorrhizal fungi are the
fungi that form a symbiotic association with the roots of 83% of dicotyledonous
plants and 79% of monocotyledons (Peterson et al. 2004). The role of mycorrhizal
fungi in increasing the absorption of nutrients is important only in ecosystems that
have nutrient deficiency (Cardoso and Kuyper 2006). These fungi can also confer
plant beneficial effects through several mechanisms (Owen et al. 2015; Rawat and
Tewari 2011; Waller et al. 2005).
In addition to negatively influencing plant growth, salinity also negatively
affects microorganisms including bacteria (Greaves 1922) and AM fungi (e.g.,
negative effect on colonization capacity, spore germination, growth of fungal
hyphae, and the
formation and function of mycorrhizal symbiosis) (Giri et al. 2007; McMillen et

al. 1998; Porcel et al. 2012; Sheng et al. 2008). Moreover, there are reports that
activity of plant growth-promoting bacteria (PGPB), such as their ability to
solubilize phosphate (Sharma et al. 2013) or produce enzyme ACC deaminase
(Upadhyay et al. 2009), is affected by environmental conditions such as salinity
stresses (Sánchez-Porro et al. 2009). Therefore, the microorganisms can increase
levels of nutrients for plants under conditions of environmental stresses that are
themselves resistant to these stresses (Etesami and Beattie 2018; Etesami and
Maheshwari 2018). It has been known that microorganisms isolated from saline
environments or halophytic plants have been able to well maintain their plant
growth-promoting (PGP) traits under salinity stress (Etesami and Beattie 2018).
These microorganisms usually have strategies to maintain their survival in saline
environments (Vreeland 1987).
Halophiles are salt-loving organisms that grow well in relatively high salt
concentrations in saline and hypersaline environments. Halophiles are present in
all major groups of microorganisms (archaea, bacteria, and eukarya), and their salt
differentiation is based on their salt tolerance level and salt needs (Ma et al. 2010).
Halotolerant or halophilic bacteria form a diverse set of microorganisms that
physi- ologically belong to different genera. Salt-resistant microorganisms usually
have strategies to maintain their survival in saline environments (Vreeland 1987).
Salinity-resistant bacteria through various mechanisms such as sodium excretion
of cells; production of extracellular polysaccharides (EPS); intracellular accumula-
tion of compatible soluble compounds, such as proline, trehalose, glycinebetaine
(GB), sucrose, and glycerol; adaptation of proteins and enzymes to high
concentrations of soluble ions; and the accumulation of K can withstand high
levels of salt (Ruppel et al. 2013). Such halotolerant PGPR have been isolated
both from halophytes (Etesami and Beattie 2018) and from salt-affected soils
(Hingole and Pathak 2016; Orhan and Gulluce 2015). These bacteria could also
increase the resistance of salinity-sensitive crop plants to salinity and improve the
growth and yield of these plants under salinity stress (Etesami and Beattie 2018).
For example, salinity-resistant bacteria with the ability to N 2 fixation or phosphate
solubilization have potential for growth and yield of crop plants in saline soils as
bio-fertilizers (Delgado-García et al. 2013). Also, these bacteria can play a special
role in counteracting environmental stresses such as salinity and drought by
producing bio-surfactants and EPS (Margesin and Schinner 2001).
AM fungi are also widely found in natural ecosystems and in salt-affected soils
(Sengupta and Chaudhuri 2002) and are considered as suitable candidates for
alleviating salinity stress in salinity-stressed plants (Garg and Chandel 2011).
Mycorrhizal fungi such as Glomus sp. and G. mosseae also occur naturally in
saline environments (Evelin et al. 2009). There are reports that salinity has not
been able to prevent AMF sporulation and colonization of AM fungi
(Aliasgharzadeh et al. 2001). Previous studies showed that AMF-inoculated plants
grew better under salinity stress compared to non-inoculated plants (Feng et al.
2002; Giri et al. 2007; Hajiboland et al. 2010; Porcel et al. 2012; Sannazzaro et al.
2007; Zuccarini and Okurowska 2008). These fungi were able to improve plant
growth, vigor, and performance and protect plant against the detrimental effects of
salinity (Evelin et al. 2009; Garg and Chandel 2011; Giri et al. 2007; Kaya et al.
2009a; Kumar et al. 2010;
Porras-Soriano et al. 2009). In general, AM fungi can increase the resistance of

AM plant to salinity by many mechanisms (including a combination of nutritional,
biochemical, and physiological effects) (Evelin et al. 2009) such as:
1. Accumulating osmoregulators (e.g., proline, glycine betaine, etc.) (Garg and
Manchanda 2009). These fungi can also synthesize trehalose in the extraradical
mycelium, which serves as the main storage carbohydrate and also as an abiotic
stress protectant (Garg and Chandel 2011; Ocón et al. 2007).
2. Improving host mineral micro- and macronutrient uptake (e.g., P, Zn, and Fe)
(Asghari 2012; Miransari and Smith 2008) and ion balance (Giri et al. 2007;
Wu et al. 2010).
3. Enhancing photosynthetic rate and water-use efficiency (WUE) (Colla et al.
2008; Wu et al. 2010).
4. Improving physiological processes such as water absorption capacity of
salinity- stressed plants (e.g., by enhancing root hydraulic conductivity, WUE,
higher K+/ Na+ ratios, and compartmentalization of sodium within some plant
tissues and favorably adjusting the osmotic balance and composition of
carbohydrates) (Al-Karaki 2006; Giri et al. 2003; Ruiz-Lozano 2003).
5. Maintaining membrane integrity that facilitates compartmentalization within
vacuoles and selective ion uptake (Rinaldelli and Mancuso 1996).
6. Lowering Na concentrations in salinity-stressed plants by dilution effects due
to growth enhancement (Al-Karaki 2006).
7. Positively influencing the composition of mineral nutrients of plants grown
under salt stress conditions (Al-Karaki and Clark 1998) by increasing and/or
selective uptake of nutrients (Porcel et al. 2012). The extensive mycelial system
of fungi can absorb nutrients such as N, P, K, Zn, Cu, and Fe. The nutrients
absorbed by AM fungi are not only for these fungi, but only some of them are
transmitted to host plant (Gosling et al. 2006).
Extensive research has been carried out on occurrence and functional diversity
of agriculturally important microbes in stressed environments as reviewed by
several authors (Grover et al. 2011; Paul 2013; Paul and Lade 2014;
Venkateswarlu et al. 2008; Yang et al. 2009). Beneficial bacteria and fungi could
improve plant performance under stress environments and, consequently,
enhance yield both directly and indirectly (Banik et al. 2006; Barassi et al. 2006;
Chakraborty et al. 2015; Choudhary 2012; Choudhary et al. 2015; Dahmardeh et
al. 2009; Damodaran et al. 2014; Davies et al. 2011; del Amor Francisco and
Cuadra-Crespo 2012; Dimkpa et al. 2009; Dolkar et al. 2018; Egamberdieva et al.
2008; Etesami and Alikhani 2016b; Fu et al. 2010; Gray and Smith 2005;
Hamilton et al. 2016; Kaymak et al. 2009; Khan et al. 2012; Mayak et al. 2004b;
Milošević et al. 2012; Nadeem et al. 2007; Paul 2012; Paul and Nair 2008;
Ramadoss et al. 2013; Rojas-Tapias et al. 2012; Shrivastava and Kumar 2015;
Soleimani et al. 2011; Tiwari et al. 2011; Upadhyay et al. 2009; Yang et al. 2009;
Yao et al. 2010; Yildirim and Taylor 2005). The main objective of the present
chapter is to highlight and discuss current knowledge on the mechanisms used by
PGPR and AM fungi to influence soil nutrient (N, P, K, and Fe) bioavailability
under salinity stress.
5.2 Salinity Stress
Among various environmental stresses, soil salinity, either resulting from natural
or man-made processes, is one of the main concerns for agriculture because it
converts arable land to nonarable land and affects crop production and agricultural
sustainability especially in arid and semiarid regions of the world (Flowers 2004;
Munns 2005). Soil salinization reduces 1–2% of the area that can be used for
agriculture each year. Approximately 7% of the land on the planet and 20% of the
total arable land are adversely affected by salinity. Soil salinity affects extensive
areas of land in both developed and developing countries. The agricultural
intensification, together with unfavorable natural conditions, has accelerated soil
salinity in many parts of the world. A soil is considered to suffer from salinity if
the electrical conductivity (EC) of its saturation is above 4 dS m —1 (America
2001), which is equivalent to approximately 40 mM NaCl (Munns and Tester
2008). Cultivated soils worldwide are becoming more saline from marginal
irrigation water, excessive fertilization, and desertification processes (Munns and
Tester 2008). The Food and Agriculture Organization (FAO) reported that more
than 1 billion ha of land throughout the world were affected by salinity (Ahmad
2013; FAO 2008). Because of global climate change, the area of land affected by
salinity is increasing day by day (Shrivastava and Kumar 2015). It has been
estimated that more than 50% of the arable land would be salinized by the year
2050 (Jamil et al. 2011).
Salinity limits the productivity of agricultural crops in varying degrees with
adverse effects on germination, plant vigor, and crop yield such as cereals (rice,
wheat, and maize), forages (clover) or horticultural crops (potatoes and tomatoes)
(Munns and Tester 2008). These crops are relatively susceptible to excessive
concentration of salts, either dissolved in irrigation water or present in soil (rhizo-
sphere) solution. At plant level, response to salinity stress is very complicated
because it reflects the combination of the effects of drought stress and the special
effect of ions. In order to understand the nature of salt stress, a definition must first
be provided. Different definitions have been made for salinity so that, according to
Shannon and Grieve (1998), salinity is the excessive concentration of soluble salts
and mineral elements in soil solution that result in salt accumulation in the root
area (rhizosphere), which makes water uptake by plant difficult. Soil salinization is
a process in which the accumulation of soluble salts in the surface layer of the soil
increases, and, as a result, the surface layer loses its potential as a growth medium
for plants. In arid and semiarid soils, the problem is excess salts, which are mainly
due to the lack of rainfall and high evaporation. Soil salinity is also due to other
causes such as excessive use of chemical fertilizers, improper water quality for
irrigation, deforestation, or compact cropping. Salinity also results in low osmotic
potential of soil solution (osmotic effect) (Munns 2005; Munns and Tester 2008),
and as a result, plants suffer from water shortages, resulting in excessive
production of reactive oxygen species (ROS) such as peroxide anions, hydroxyl
radical, hydrogen peroxide, and single oxygen, each of which can disrupt normal
plant metabolism and lead to the destruction of plasma membranes and internal
membrane systems (Parida and Das 2005). It has been widely reported that
salinity limits plant growth and
development, which leads to changes in physiology, morphology, and biochemical

properties of plants. In general, salinity-induced stress reduces the yield of many
crop plants because salt inhibits plant photosynthesis, protein synthesis, lipid
metabolism, plant biomass, green pigments, stomatal conductance, and
transpiration rate and lead to change in activity of enzymes such as superoxide
dismutase (SOD), peroxidase (POD), ascorbate peroxidase (APX) and catalase
(CAT), and osmolyte accumulation (such as proline, glycine betaine, total free
amino acids, soluble sugars, and so on). In salinity stress conditions, seed
germination stage, as one of the most important plant life stages, which plays an
important role in plant establishment, is negatively affected by salinity. Salinity
also leads to an imbalance of phytohormones (in particular IAA and ethylene) and
thus decreases plant growth (Kaya et al. 2009b). High concentrations of soluble
salts and some ions (Na+ and Cl—), due to causing specific ion effects (mainly Na +
and Cl—) (specific ion effect), which result in nutritional imbalances or ion
cytotoxicity (Munns 2005; Munns and Tester 2008), undesirably also affect plant
growth by limiting the absorption and transfer of essential nutrients to plant roots
(Shrivastava and Kumar 2015), resulting in deficiency symptoms, and reduce the
availability of nutrients (N, P, K, Ca, Mg, Fe, Cu, Zn, etc.) in soil (Barea et al.
2005; Moradi et al. 2011). Almost all micro- and macronutrient contents decrease
in the roots and shoots of the plant with increasing NaCl concentration in the
growth medium (Paul and Lade 2014).
In general, one of the most important consequences of salinity is the nutritional
imbalances or ion cytotoxicity. The imbalance of nutrients, in turn, leads to a
decline in the growth and development of plants. Plant nutrient management is the
most practical and easiest way to overcome stress. The nutritional status of the
plant mainly affects their ability to adapt to adverse environmental conditions and
in particular non-biological stress factors. Several studies have shown that plants
exposed to environmental stresses need the higher amount of nutrients to adapt to
stress and reduce the negative effects of these stresses. In addition to having toxic
effects on plant cells, soil nutrient imbalances can affect the plant’s ability to
survive or absorb water (Etesami 2018; Etesami and Maheshwari 2018). However,
it has been found that salinity-resistant microorganisms can grow well in salt and
high osmotic pressure conditions and partially meet the nutritional needs of the
plant under salinity stress (Fig. 5.1 and Table 5.1) (Etesami and Beattie 2018).
5.3 PGPR and AM Fungi-Mediated Increase of N

Availability Under Salinity Stress
Nitrogen (N) is the most vital nutrient for plant growth and productivity. Although
there is about 78% N2 in the atmosphere, soil N is mostly in organic forms and
unavailable for plants. Deficiency of this nutrient in the soil results in a significant
reduction in plant growth and yield. As mentioned above, one of the adverse
effects of soil salinity on plants is to alter the uptake of nutrients by plants
(decrease in uptake of nutrients with increase in soil salinity) (Cheng-Song et al.
2010; Rawal and Kuligod 2014). Studies indicate that salinity reduces N
uptake/accumulation (Feigin
Fig. 5.1 An overview on the role of PGPR and mycorrhizal fungi to promote nutrient acquisition
1985). One of the ways to alleviate, to some extent, the detrimental effects of
salinity and help to improve the yield of crops is to use chemical fertilizers.
According to Rawal and Kuligod (2014), under salinity conditions, application of
higher doses of N resulted in increased yield. In general, in most soils of saline
and drought areas, the available N shortage for plants is present, and this shortage
cannot be compensated for by using only chemical fertilizers at global level. On
the other hand, the use of biological nitrogen fixation (BNF) process is more
efficient and more favorable than chemical fertilizers (Shamseldin and Werner
2005). The atmospheric N2 is converted into plant-utilizable forms by BNF which
changes N2 to ammonia (NH4+) by nitrogen-fixing PGPR using a complex enzyme
system known as nitrogenase (Kim and Rees 1994). The importance of this
process is saving on the use of chemical fertilizers, providing N in line with the
plant’s requirements and, consequently, increasing plant yield. Also, the
excessive use of bio-fertilizers does not create environmental problems unlike
chemical fertilizers. On the other hand, following the planting of leguminous
plants, the soil is enriched in terms of N absorption, and the remaining effects of
leguminous plants will be useful for subsequent planting (Shamseldin and Werner
2005). Today, in planning for sustainable agricultural systems, the use of this
type of symbiosis is considered a basic necessity.
It is known that most legume plants are sensitive or relatively resistant to
salinity (Dulormne et al. 2010; Garg and Chandel 2011; Jebara et al. 2010; Khadri
et al. 2006; López and Lluch 2008). These plants are dependent on nitrogen
fixation for their optimal growth (Chalk et al. 2010; Jebara et al. 2010). Salinity, in
addition to its
Table 5.1 Potential application of PGPR and mycorrhizal fungi to improve nutrient availability to
salinity-stressed plants
Amelioration effect of
Experimental microorganism on
Nutrient plant(s) Microorganism(s) salinity-stressed plant References
N Cajanus Glomus mosseae The symbiotic Garg and
cajan (L.) association with AM Chandel
led to significant (2011)
improvement in plant
dry mass and nitrogen-
fixing potential of
nodules under salt
stress. AM plants had
lower trehalase activity
under saline and
non-saline conditions
P, K, Acacia Glomus fasciculatum Mycorrhizal plants Giri et al.
Zn, and nilotica maintained greater root (2007)
Cu and shoot biomass at all
salinity levels
compared to
non-mycorrhizal plants.
AM-inoculated plants
had higher P, Zn, and
Cu concentrations than
un-inoculated plants
Mycorrhizal plants
accumulated a higher
concentration of K at all
salinity levels.
Mycorrhiza-inoculated
plants had lower
concentration of Na in
shoot tissue.
Mycorrhizal fungus
alleviated deleterious
effects of saline soils on
plant growth that could
be primarily related to
improved P nutrition.
The improved K+/Na+
ratios in root and shoot
tissues of mycorrhizal
plants may help in
protecting disruption of
K-mediated enzymatic
processes under salt
stress conditions
P, K, Soybean Glomus etunicatum Soybean plants Sharifi et al.
and Zn (Glycine max inoculated with the AM (2007)
L.) fungus had significantly
higher fresh and dry
(continued)

weight, root proline, P,
K and Zn compared to
non-AM plants
P, N, Sesbania Glomus macrocarpum Mycorrhizal seedlings Giri and
and Mg aegyptiaca had significantly higher Mukerji
and root and shoot dry (2004)
S. grandiflora biomass production
than non-mycorrhizal
seedlings grown in
saline soil. The content
of chlorophyll was
greater in the leaves of
mycorrhiza-
inoculated seedlings as
compared to
un-inoculated
seedlings. The number
of nodules was
significantly higher in
mycorrhizal plants than
non-mycorrhizal plants.
Mycorrhizal seedling
tissue had significantly
increased
concentrations of P, N,
and Mg but lower Na
concentration than
non-mycorrhizal
seedlings
N Cajanus Glomus mosseae AM significantly Garg and
cajan (L.) improved nodulation, Manchanda
Mill sp. leghemoglobin content, (2008)
and nitrogenase activity
under salt stress.
Activities of superoxide
dismutase (SOD),
catalase (CAT) and
peroxidase (POX), and
glutathione reductase
(GR) increased
markedly in
mycorrhizal-stressed
plants
P Phyllanthus Acinetobacter sp. and Both bacteria alone or Joe et al.
amarus Bacillus sp. in combination (2016)
promoted a higher vigor
index, germination (%),
plant biomass, P
(continued)

content, plant phenolic
content, radical
scavenging, and
antioxidative activity,
compared to
un-inoculated control
N, K, Wheat Bacillus pumilus, Wheat root dry weight Upadhyay
and P (Triticum B. aquimaris, and shoot biomass, and Singh
aestivum L.) B. arsinicus, proline and total (2015)
Arthrobacter sp., soluble sugar
B. cereus, accumulation, and
P. mendocina, and percentage of N, K, and
B. subtilis P in leaves of wheat
increased significantly
after inoculation with
PGPR, as compared to
un-inoculated plants.
These PGPR showed
maximum reduction of
Na content in wheat
leaves of about 23% at
both 60 and 90 days
after sowing and
produced the best yield
of around 17.8% more
than the control
N and P Salicornia Azospirillum At the end of the Bashan
bigelovii halopraeferens, growing season, the N et al. (2000)
Azospirillum and protein content of
brasilense, Vibrio seeds significantly
aestuarianus, Vibrio increased. The P
proteolyticus, Bacillus content in foliage
licheniformis, and increased significantly
Phyllobacterium sp. in plants treated with
bacterial strains
P Avicennia Oceanobacillus O. picturae El-Tarabily
marina picturae significantly increased and Youssef
available P, decreased (2010)
pH, positively
enhanced nutrient
uptake parameters in
roots and shoots,
increased stem
circumference, number
of xylem vessels, mean
xylem diameter, and
the hydraulically
weighted xylem vessel
diameter, compared
with
non-inoculated plants
(continued)

N, P, K, Groundnut Brachybacterium Plant length, root Shukla et al.
and Ca (Arachis saurashtrense (JG-06), length, shoot dry (2012)
hypogaea L.) Brevibacterium casei weight, root dry
(JG-08), and weight, and total
Haererohalobacter biomass were
(JG-11) significantly higher in
inoculated plants
compared to
un-inoculated plants.
The PGPR-inoculated
plants were quite
healthy and hydrated,
whereas the
un-inoculated plant
leaves were desiccated
in the presence of
100 mM NaCl. The
inoculated plants also
had a higher K+/Na+
ratio and higher Ca2
+
, P, and N content
N, P, Maize (Zeya Pseudomonas and Under stress conditions, Nadeem
and K mays L.) Enterobacter spp. more N, P, and K et al. (2009)
uptake and high K+/Na+
ratios were recorded in
inoculated plants
compared with the
control
N Peanut Klebsiella, A significant increase in Sharma
Pseudomonas, total nitrogen et al. (2016)
Agrobacterium, and (N) content (up to 76%)
Ochrobactrum was observed over the
non-inoculated control.
Under salt stress,
inoculated peanut
seedlings maintained
ion homeostasis,
accumulated less
reactive oxygen species
(ROS), and showed
enhanced growth
compared to
non-inoculated
seedlings
K and Wheat Bacillus licheniformis Inoculation of Singh and
Ca HSW-16 B. licheniformis Jha (2016)
HSW-16 protected
wheat plants from
growth inhibition
(continued)

caused by NaCl and
increased plant growth
(6–38%) in terms of
root length, shoot
length, fresh weight,
and dry weight. Ionic
analysis of plant
samples showed that
the bacterial
inoculation decreased
the accumulation of
Na+ content (51%) and
increased K+ (68%) and
Ca2+ content (32%) in
plants at different
concentration of NaCl
N, K, P, Strawberry Bacillus subtilis EY2, PGPR inoculations Karlidag
Ca, B. atrophaeus EY6, significantly increased et al. (2013)
Mg, S, B. sphaericus EY30, the growth, chlorophyll
Mn, Cu, Staphylococcus kloosii content, nutrient
and Fe EY37, and Kocuria element content, and
erythromyxa EY43 yield of strawberry
plants. The highest N,
K, P, Ca, Mg, S, Mn,
Cu, and Fe
concentrations were
observed in the
inoculated plants
K, Ca, Pea (Pisum Variovorax paradoxus V. paradoxus 5C-2 Wang et al.
Mg, and sativum L. cv. 5C-2 increased K, Ca, Mg, (2016)
P Alderman) and P uptake and root
to shoot K flow but
decreased Na flow and
increased Na
deposition in roots.
Thus, shoot K+: Na+
ratio increased
following V.
paradoxus
5C-2 inoculation
N, P, Wheat Pseudomonas putida, Inoculation with the Nadeem
and K Enterobacter cloacae, PGPR resulted a et al. (2013)
Serratia ficaria, and significant increase in
Pseudomonas the growth and yield
fluorescens parameters of wheat.
The inoculated plants
also improved the
nutrient status of the
wheat plants. The
(continued)

inoculated plants had
low Na and high N, P,
and K contents
N, P, K, Cotton Raoultella planticola Raoultella planticola Wu et al.
Ca, and reduced the quantities (2012)
Fe of ethylene and abscisic
acid in cotton seedlings
and increased indole-3-
acetic acid content in
cotton seedlings under
salinity stress. The
accumulation of N,
P, K, Ca, and Fe in the
cotton plants was
increased significantly
in Raoultella planticola
treatment, whereas the
uptake of Na in cotton
seedlings decreased
K, Ca, Maize (Zea Azotobacter sp. C5 Chlorophyll, Mg, K, Rojas-
and Mg mays L.) Ca, Mg, total Tapias et al.
polyphenol, and proline (2012)
of the inoculated plant
increased
References: Bashan et al. (2000), El-Tarabily and Youssef (2010), Garg and Chandel (2011),
Garg and Manchanda (2008), Giri et al. (2007), Giri and Mukerji (2004), Joe et al. (2016),
Karlidag et al. (2013), Nadeem et al. (2009, 2013), Rojas-Tapias et al. (2012), Sharifi et al.
(2007), Sharma et al. (2016), Shukla et al. (2012), Singh and Jha (2016), Upadhyay and Singh
(2015), Wang et al. (2016), and Wu et al. (2012)
negative effect on plant growth, has a negative effect on the nitrogen fixation
process, such as nodule growth (Abdelmoumen and El Idrissi 2009), symbiotic
activity (Dulormne et al. 2010; Jebara et al. 2010), activity of the nitrogenase
enzyme (Jebara et al. 2010), nodule respiration (Dulormne et al. 2010; López and
Lluch 2008), nodule establishment (Aydi et al. 2008), leghemoglobin, acetylene-
reduction activity, and nitrogen content of legume plants (Garg and Chandel
2011), for example, in soybean (Glycine max) (van Hoorn et al. 2001), mung bean
(Vigna mungo L. Hepper) (Mensah and Ihenyen 2009), common bean (Phaseolus
vulgaris), faba bean (Vicia faba) (Rabie and Almadini 2005), and goat’s rue
(Galega officinalis) (Egamberdieva et al. 2013; Paul and Lade 2014).
In addition to the effect of salinity on the nitrogen fixation process, salinity also
affects the establishment and activity of the legume-Rhizobium, which is
susceptible to salinity (Jebara et al. 2010). It is known that environmental stresses
including salinity stress have a negative effect on the number of rhizobial isolates,
BNF capacity (Duzan et al. 2004), and the ability to produce some bacterial
metabolites
(Sánchez-Porro et al. 2009; Upadhyay et al. 2009; Yoon et al. 2001). There are
different rhizobial strains in soil that their effect on their host is not the same in
terms of BNF and dealing with environmental stresses (Rehman and Nautiyal
2002). In order to obtain the best bio-fertilizers, the exact identification of the
isolates of each region and their biological ecology, the isolation of the specific
rhizobial isolates of each plant, and the adaptation of these rhizobial isolates to
different climatic conditions are necessary. Therefore, selection and breeding of
genotypes and halotolerant rhizobial strains that can grow under stress conditions
might be an effective tool at resolving the soil reclamation practices.
The combined use of AM fungi with rhizobial bacteria has also been suggested
as an effective strategy to increase plant growth and nitrogen fixation under
salinity stress (Chalk et al. 2006; Franzini et al. 2010; Garg and Chandel 2011).
AM fungi could neutralize harmful effects of salinity on nodulation and nitrogen
fixation and thereby alleviate the salinity-induced premature nodule senescence
(Garg and Chandel 2011; Garg and Manchanda 2008, 2009; Goss and De
Varennes 2002; Patreze and Cordeiro 2004) by different ways such as (i)
increasing the fitness of host plants by enhancing shoot and root biomass (Garg
and Chandel 2011);
(ii) enhancing host plant P nutrition and other nutrients with low mobility, such as
Fe, Cu, and Zn (Kaya et al. 2009a; Miransari and Smith 2008); (iii) decreasing
uptake of Na by salinity-stressed plant (Al-Karaki 2006; Chakraborty et al. 2008;
Giri et al. 2007); and (iv) stimulating the salinity-induced accumulation of
trehalose, a carbohydrate in osmoprotection and osmotic adjustment against
salinity stress, by inhibiting trehalase activity in AM plants and increasing total
soluble sugars (Garg and Chandel 2011).
One of the responses of salinity-stressed plants (osmotic adjustment) against
salt stress is various organic compounds, collectively known as compatible solutes
or osmolytes (Contreras-Cornejo et al. 2009; Cortina and Culiáñez-Macià 2005).
These compounds play an important role as an abiotic stress protectant in a wide
variety of organisms (Contreras-Cornejo et al. 2009; Elbein et al. 2003; Fernandez
et al. 2010; Garg and Chandel 2011). Trehalose (α-D-glucopyranosyl-1,1-α-D-
glucopyranoside) is one of these osmolytes that has been detected in symbiotic
nitrogen-fixing bacteria such as Rhizobium (the accumulation in bacteroids and in
nodules of leguminous plants) (Müller et al. 2001). This compatible solute plays
an important role in the maintenance of efficient nitrogen fixation, protection of
bacterial nitrogenase activity, and whole plant tolerance under drought and
salinity stresses (Farías-Rodríguez et al. 1998; Garg and Chandel 2011; López et
al. 2008; Zacarías et al. 2004). The ability of AM fungus has been shown to
increase plant nitrogen content under saline conditions. For an example, in a
study, Giri and Mukerji (2004) showed that AM-inoculated plants had
significantly greater concentration of N and the greater number of nodules than
non-mycorrhizal plants under salinity stress. Increased N concentration under
saline conditions may help to decrease Na uptake, which may be indirectly related
to maintaining the chlorophyll content of the plant (Giri and Mukerji 2004).
Improved nodulation and N fixation in mycorrhizal plants may be because of
alleviation from P stress and possibly to absorption of some essential
micronutrients, which leads both to enhanced growth of plants and has an indirect
effect on the N-fixing system (Founoune et al. 2002).
Environmental conditions such as stresses affect the production of extracellular

polysaccharides (EPS) of rhizobia strains, so that these strains produce more EPS
to withstand adverse environmental conditions (Ashraf et al. 2004; Delavechia et
al. 2003). It has been reported that salinity- and drought-tolerant rhizobial strains
produce more EPS content and, by increasing the amount of EPS, tolerate unsatis-
factory conditions and continue to grow (Ashraf et al. 2004; Delavechia et al.
2003). On the other hand, the survival of rhizobial strains in soil depends on the
ability of these strains to bind to the host plant and to create a symbiotic
relationship. Among these, EPS are of particular importance in the specialization
of rhizobia in identifying these strains by the host plants (Werner 1992). The EPS
of the rhizobial strains play an important role in the process of recognizing
legume-rhizobium as well as protecting the bacterial cell against environmental
stresses (Werner 1992). There- fore, EPS-producing salinity-resistant rhizobial
strains can not only tolerate the conditions of salinity stress but can also act more
successful in creating a symbiotic relationship with the host plant than salinity-
sensitive rhizobial strains. In several experiments conducted in salinity and
drought regions, it was observed that the salinity- and drought-resistant rhizobial
isolates isolated from salt-affected soils were of significant efficiency (Shamseldin
and Werner 2004, 2005).
Since essential plant nutrients are taken up from the soil by roots (Mills et al.
1996), good root growth is considered a prerequisite for enhanced plant develop-
ment. The morphological modification of roots plays an important role in the
mechanisms of stress response (Carmen and Roberto 2011). Microorganisms
increase root system of plants by production of phytohormone IAA and ACC
deaminase. In addition to the production of IAA, gibberellins and other growth
regulators produced by PGPR can support the increase of root length, root surface
area, and number of root tips, leading to enhanced uptake of nutrients, thereby
improving plant health under stress conditions (Egamberdieva and Kucharova
2009; Etesami and Maheshwari 2018). Rhizobacteria-mediated root proliferation
has been well proved, and it also works in stressed soils (Diby et al. 2005a).
Inoculation of various plant species with PGPR has also reported to lead to
enhanced formation of lateral roots and root hairs that can result in enhanced
tolerance to abiotic stress (Etesami and Maheshwari 2018; Paul and Lade 2014).
Promotion of root growth results in a larger root surface and can, therefore, have
positive effects on water acquisition and nutrient (i.e., N) uptake (Diby et al.
2005b; Paul and Sarma 2006) that is expected to alleviate the stress effects in the
plant (Chakraborty et al. 2006; Hamdia et al. 2004; Long et al. 2008; Paul and
Sarma 2006). Microbial IAA is involved in many processes of nodule formation
by rhizobia in legume plants, such as founder cell specification, nodule initiation
and differentiation (IAA accumulation), nodule numbers, vascular bundle
formation, and cell division and differentiation (Etesami et al. 2015b; Etesami
and Beattie 2017). These three later events are more necessary for nodule
formation (Glick 2012; Theunis 2005). In addition, due to having the function in
increased root system, IAA-producing bacteria can provide more number of active
sites and access to colonization for N2-fixing bacteria or PGPR.
Previous studies indicate that salinity can either decrease (300 mM NaCl)
(Dunlap and Binzel 1996) or increase (100 mM NaCl) (Albacete et al. 2008) root
IAA accumulation in plant, which might affect cell elongation and root growth. It
has been known that the bacteria isolated from saline environments have been able
to produce IAA in the presence of salinity (Etesami and Beattie 2018). In a study,
Sadeghi et al. (2012) demonstrated that a Streptomyces isolate increased plant
growth in wheat and produced IAA in the presence of salt. The ability to modify
plant stress levels by providing IAA, a molecule involved in the development of
lateral roots, has also been reported for halotolerant bacteria isolated from saline
habitats and halophytes (Bian et al. 2011; Marasco et al. 2012; Naz et al. 2009;
Piccoli et al. 2011; Sgroy et al. 2009; Siddikee et al. 2010; Tiwari et al. 2011).
Arthrobacter sp., Nitrinicolalacis aponensis, Brachybacterium sp.,
B. saurashtrense, Brevibacterium casei, Br. halotolerans, Haererohalobacter sp.,
Klebsiella sp., Pseudomonas sp., P. stutzeri, P. pseudoalcaligenes, P. putida,
P. mendocina, Agrobacterium tumefaciens, Ochrobactrum anthropi, Bacillus sp.,
B. cereus, B. pumilus, B. simplex, B. mycoides, B. aquimaris, B. licheniformis,
B. mycoides, B. subtilis, Sporosarcina aquimarina, Serratia marcescens,
S. plymuthica, S. plymuthica, Thalassospira permensis, Acinetobacter,
Microbacterium sp., M. oxydans, Streptomyces sp., S. avidinii, S. europaeiscabiei,
S. exfoliatus, S. umbrinus, S. griseoplanus, Rhodococcus sp., R. equi,
R. erythropolis, Micrococcus luteus, Marinococcus halophilus, Nocardia sp.,
Halomonas sp., H. elongata, H. eurihalina, H. sinaiensis, H. halmophila,
H. ilicicola, H. indalina, H. variabilis, H. xinjiangensis, H. taeheungii,
Halobacillus trueperi, Nesterenkonia halobia, Oceanobacillus picturae,
Kushneria, Virgibacillus olivae, Lysinibacillus fusiformis, Achromobacter
xylosoxidans, Mesorhizobium sp., Zhihengliuella sp., Vibrio alginolyticus, and
Cronobacter sakazakii are some examples of IAA-producing salt-tolerant PGPR
isolated from halophytes (Gontia et al. 2011; Mapelli et al. 2013; Sgroy et al.
2009; Sharma et al. 2016; Shukla et al. 2012; Tiwari et al. 2011). According to the
above studies, it can be concluded that salinity-resistant rhizobacteria or rhizobial
bacteria with the ability to produce IAA may help to increase the resistance of
plants to salinity stress and increase the amount of N in the plants.
One of the responses of plants under stress conditions such as salinity stress is
the increase in the level of intracellular ethylene inside the plant (stress ethylene).
Stress ethylene reduces the vegetative stage of plant growth and eventually
decreases the plant yield (Etesami and Maheshwari 2018; Glick 2005). Siddikee et
al. (2011) also stated that the ethylene produced in response to salinity stress
reduced root growth and thus reduced water and nutrient uptake and finally
decreased plant growth. Previous researchers found that formation and function of
nitrogen-fixing nodules on legume roots were severely inhibited by addition of
exogenous ethylene (Peters and Crist-Estes 1989). Ethylene inhibits the elongation
of infection threads and, consequently, the formation of nodules in most legumes
(Etesami et al. 2015b; Sugawara et al. 2006). In addition, production of ethylene, a
signal molecule for induced systemic resistance in plants, decreases endophytic
colonization in plants (Iniguez et al. 2005). The overproduction of ethylene can
also cause the inhibition of
root elongation, lateral root growth, and root hair formation (Belimov et al. 2009;
Mayak et al. 2004b; Saleem et al. 2007), which subsequently results in decreasing
the nodule number of on root. Some soil bacteria produce ACC deaminase
enzyme. This enzyme converts ACC (a substrate for ethylene production) to α-
ketobutyrate and ammonium. By modifying the ACC production in plants, ACC
deaminase- producing bacteria can prevent the excess ethylene production in the
plant (Glick 2014). The ACC deaminase trait has been extensively studied in
numerous soil microbial species, that is, bacteria, fungi, and endophytes; however,
this trait is most common among PGPR (Etesami and Maheshwari 2018; Glick
2005) such as the genera Achromobacter, Acidovorax, Alcaligenes, Enterobacter,
Klebsiella, Methylobacterium, Pseudomonas, Rhizobium, and Variovorax
(Esquivel-Cote et al. 2010). Ahmed et al. (2004) found that ACC deaminase-
producing bacteria increased grain yield, root weight, root length, and more
nitrogen uptake in straw and wheat grain by decreasing stress ethylene level
compared to control.
Salinity has been shown to cause PGPR to lose their ACC deaminase enzyme
production (Upadhyay et al. 2009). However, it has been found that ACC
deaminase-producing salt-tolerant PGPR can survive well in a saline environment
and that their beneficial properties help plants to overcome stress effects by
reducing ethylene levels (Mayak et al. 2004a). The production of enzyme ACC
deaminase has also been well reported in halotolerant bacteria isolated from
halophytic plants and from saline environments (Jha et al. 2012; Siddikee et al.
2010; Zhou et al. 2017). The roots of halophytes may be associated with
promising ACC deaminase- producing bacterial candidates for promoting growth
and salt tolerance in crops (Etesami and Beattie 2018). For example, novel
diazotrophic halotolerant bacteria from roots of Salicornia brachiata featured
ACC deaminase activity and these isolates included Brachybacterium
saurashtrense, Brevibacterium casei, Cronobacter sakazakii, Haererehalobacter,
Halomonas, Mesorhizobium, Pseudo- monas, Rhizobium radiobacter, Vibrio, and
Zhihengliuella (Jha et al. 2012). Examples of halotolerant ACC deaminase-
producing PGPR include Micrococcus yunnanensis, Planococcus rifietoensis,
Variovorax paradoxus, Brachybacterium saurashtrense, Klebsiella sp.,
Pseudomonas sp., P. stutzeri, P. putida, Agrobacterium tumefaciens,
Ochrobactrum anthropi, Serratia marcescens,
S. plymuthica, Thalassospira permensis, Microbacterium sp., M. oxydans, Bacillus
sp., B. cereus, B. licheniformis, B. pumilus, B. subtilis, B. mycoides, S. plymuthica,
M. oxydans, Microbacterium sp., Streptomyces sp., Rhodococcus sp., Rh.
erythropolis, Nocardia sp. Halomonas taeheungii, H. xinjiangensis,
Brevibacterium halotolerans, Achromobacter xylosoxidans, Zhihengliuella sp.,
Mesorhizobium sp., Brachybacterium sp., Vibrio alginolyticus, Brevibacterium
casei, Cronobacter sakazakii, P. pseudoalcaligenes, Haererehalobacter sp.,
Pantoea agglomerans,
P. oryzihabitans, and Halomonas sp. (Gontia et al. 2011; Jha et al. 2012; Mapelli
et al. 2013; Sgroy et al. 2009; Sharma et al. 2016; Szymańska et al. 2016; Teng et
al. 2010; Zhou et al. 2017), which were isolated from species of halophytes.
Generally, it seems that the production of IAA and ACC deaminase by salinity-
tolerant PGPR might be an important tool in salt tolerance of plants/legumes in
salt-affected soils (Etesami and Beattie 2018; Etesami and Maheshwari 2018).
5.4 PGPR and AM Fungi-Mediated Increase of P

Phosphorus (P) is an important and essential macronutrient for plants and

microorganisms that its shortage restricts plant growth and development and,
unlike N, does not have a large atmospheric source (Katznelson et al. 1962). Stem
development, root and shoot firmness, fixation of nitrogen in legumes,
macromolecu- lar biosynthesis, improvement in crop quality, production and
transfer of energy, photosynthesis, and resistance to plant diseases are related to P
nutrition (Roychoudhury and Kaushik 1989). The deficiency of P supply and
availability also remains a severe limitation on nitrogen fixation and symbiotic
interactions (Pereira and Bliss 1989). In contrast to N, phosphate compounds are
relatively insoluble and therefore are not easily leached from the soil profile.
Usually, low amounts of P in soils and its tendency to react with soil constituents
and the production of relatively insoluble compounds and therefore nonabsorbable
compounds for plants make P very important for soil fertility. It is worth
mentioning that the total amount of P in soil is much more than available P, but
the importance of the available P in plant growth is higher. Phosphorus is
predominantly found in mineral soil parts, either as adsorbed on mineral surfaces
of soil or as relatively soluble sediments, or in organic forms that are either as
adsorbed on mineral surfaces of soil, or as a part of microbial biomass or with
organic matters. Phosphorus is extracted from phosphate rock (over 80% of
phosphate rock reserves are utilized for fertilizer production) (Owen et al. 2015),
which is a nonrenewable resource. This is very important for a number of
countries without phosphate rock (Van Vuuren et al. 2010). The extraction of P
minerals and spread of P fertilizers in agricultural land are not sustainable due to
the limited resources of P, and this will make production of this fertilizer in the
future difficult. In addition, in practice, P use efficiency (recovery of fertilizer P) is
between 10% and 25%. That is, about 75% of this fertilizer in soil is converted
into insoluble forms by reacting with metal cations (formation of complexes with
Fe3+, Al3+ and Ca2+) (Gyaneshwar et al. 2002; Stevenson and Cole 1999).
Plants absorb P mainly as primary and secondary ions of orthophosphates
(H2PO4— and HPO42—), which are present in the soil solution. The concentration of
these ions in the soil solution at any time is negligible (Marschner 1995) and often
is less than 0.1 mg L—1. The P in the soil solution should be renewed continuously;
otherwise the plant will not have sufficient P to complete its growth. The
concentration of various P ions in soil solution is closely related to the pH of
environment. Acidic environments are suitable for H2PO4— ions and pH-
containing environments higher than 7 for HPO42— ions. According to a general
experimental law, the maximum usable P for most agricultural plants is when the
soil pH is in the range of 5.5–7. The P in calcareous soils is converted into
insoluble calcium and magnesium compounds and in acid soils into iron and
aluminum phosphates, thereby reducing its access to plants. In general, different
forms of P in soil are controlled by the soil’s natural properties, including pH, the
soluble and exchangeable cations (Ca2+, Mg2+, Fe2+, etc.), the type of soil particles,
and their surface (Penfold 2001).
Salinity also reduces phosphorus (P) uptake/accumulation in crops grown in

soils primarily by reducing P availability (Etesami and Maheshwari 2018; Paul
and Lade 2014) because phosphate ions precipitate with Ca+2 ions (Navarro et al.
2001; Parida and Das 2005; Rogers et al. 2003). In addition, the reduction in P
availability in saline soils was suggested to be a result of ionic strength effects that
reduce the activity of phosphate and the tight control of P concentrations by
sorption processes and by low solubility of Ca-P minerals. In saline soils, due to
the presence of cations (e.g., Ca2+ and Mg2+) in high concentrations, it is possible
to form insoluble cation- phosphorus compounds in salt-affected soils (Etesami
and Maheshwari 2018). Previous studies also showed that salinity could reduce
the P uptake by plant (Barea et al. 2005; Patel et al. 2010). For example, Patel et
al. (2010), in a study, showed that salinity reduces the P uptake by plant (Acacia
auriculiformis A. Cunn. Ex Benth). In addition to forming insoluble cation-
phosphorus compounds, decrease in the P uptake by plant under salinity stress can
also be associated with the poor root development (Rawal and Kuligod 2014).
One of the ways to meet the P requirement of plants in saline or non-saline
soils is to use chemical fertilizers; however, due to their limited resources, the
increase in their cost, the environmental hazards resulting from their application,
and the fixation of a large part of the P fertilizers consumed as insoluble forms for
plant, attention to use of phosphate bio-fertilizers has been increasing in the past
decades. It is well found that soil microorganisms (bacteria, fungi, actinomycetes,
and even algae) interfere with some of the solubilizing processes of phosphate,
which affect the transformation and maintenance of the status of P and ultimately
its bioavailability for the plant (Richardson 2001; Sharma et al. 2013).
It is well known that various PGPR can increase the availability of nutrients to
plant. For example, phosphate-solubilizing microorganisms (PSMs) provide P
available to plants by different mechanisms (Sharma et al. 2013). There is
evidence that soil phosphate-solubilizing bacteria (PSB) can solubilize and convert
insoluble phosphorus into available forms to plant. Also, microbial biomass with
absorption of soluble phosphorus prevents precipitation or fixation of P in the soil
(Khan et al. 2007).
PSMs form a significant part of the population of soil microorganisms (Kucey
et al. 1989). Bacteria and fungi account for the highest percentage of PSMs in soil;
therefore they are divided into two groups of phosphate-solubilizing bacteria
(PSB) and phosphate-solubilizing fungi (PSF) (Whitelaw et al. 1997). PSB can
solubilize insoluble P compounds and release P from these compounds (Sharma et
al. 2013). The most important types of PSB can be referred to Enterobacter
agglomerans, Bacillus circulans, B. subtilis, B. megaterium var phosphaticum,
Pseudomonas putida, P. fluorescens, P. striata, Pantoea, Paenibacillus polymyxa,
Rhizobium leguminosarum bv. trifolii, Xanthobacter agilis, Klebsiella, and
Agrobacterium radiobacter, and fungi Aspergillus and Penicillium are of the most
important types of PSF (Sharma et al. 2013). It has been also reported that PSF
produce more acids compared to PSB (Venkateswarlu et al. 1984) and are able to
traverse long distances more easily than PSB and hence may be more important to
P-solubilization in soils (Kucey 1983). Overall, due to having a higher population
density, bacteria may be very effective at solubilizing phosphates compared to
fungi.
The solubilization and mineralization of P in the rhizosphere is the most impor-

tant mechanism of PGPR including PSB that provide plants with the nutrient. PSB
play an important role in three main components of soil P cycles such as
dissolution- precipitation, absorption and desorption (interactions between mineral
surfaces and P), and mineralization-immobilization (transformation of organic P to
inorganic P by biological transformations) (Gyaneshwar et al. 2002; Jones and
Oburger 2011; Owen et al. 2015). PSB and their interactions with soil play a
critical role in mediating the distribution of P between the soluble P reservoir in
the soil solution and the total P of the soil through solubilization and
mineralization reactions, the immobilization of P into the microbial biomass, or
the formation of relatively available organic P and mineral forms. In general, PSB
convert insoluble phosphate compounds into soluble forms by producing and
releasing metabolites such as organic acids that, through their hydroxyl and
carboxyl groups, chelate the cations (mainly calcium) bound to phosphate (Miller
et al. 2010; Sagoe et al. 1998).
Some of the potential known mechanisms through which PSB could mobilize
the soil P unavailable for plants include:
1. Acidification of rhizosphere medium by production of mineral acids and H +

extrusion or NH4+ absorption (release of H+ ions from the roots during the
assimilation of NH+ 4) (Illmer and Schinner 1992).
2. Exchange reactions. In this process, the low molecular weight organic anions
(e.g., succinic, citric, gluconic, α-ketogluconic, and oxalic acids) produced by
PSB are exchanged for P on adsorption sites of soil (Chen et al. 2006; Jones
and Oburger 2011; Zhang et al. 2014). The organic acids/organic anions (e.g.,
lactic acid, tartaric acid, aspartic acid, gluconic acid, oxalic acid, and citric
acid) produced by PSB can also lower pH, compete with P for adsorption sites
on the soil, and form soluble complexes with metal ions associated with
insoluble P (Ca, Al, and Fe) (Sharma et al. 2013).
3. Releasing CO2 during respiration. The formed carbonic acid caused by being
dissolved CO2 in water (present in the soil pores) can solubilize P by
diminishing the mycorrhizosphere pH (Marschner 1995).
4. Stimulating the indirect dissolution of calcium phosphate (Ca-P) by removing
and assimilating phosphate from the soil (sink theory) to re-establish the P
equilibrium (Halvorson et al. 1990).
5. The release of chelating compounds (e.g., siderophores, enzymes, phenols,
amino acids, sugars, and organic acid anions). These compounds reduce metals
with variable oxidation states, which bound to phosphate, to a lower oxidation
state, resulting in more soluble phosphate (Kim et al. 1997).
6. The secretion of extracellular alkaline and acid phosphatases or phytases (enzy-
matic hydrolysis), which convert organic phosphate into an inorganic form
(Etesami and Maheshwari 2018; Franco-Correa et al. 2010; Gyaneshwar et al.
2002; Owen et al. 2015; Sharma et al. 2013).
It has been reported that the main mechanism for mineralization of organic P is
the production of acid phosphatases (Khan et al. 2009; Sharma et al. 2013).
Species
of genera Bacillus, Burkholderia, Enterobacter, Pseudomonas, Rhizobium,

Serratia, and Staphylococcus are the most important bacteria involved in P
mineralization (Shedova et al. 2008).
Previous studies have shown that PSB have also other PGP traits (Etesami and
Maheshwari 2018; Sharma et al. 2013). Based on scientific findings, plant growth-
promoting bacteria (PGPB) probably have more than one mechanism for plant
growth (Etesami and Maheshwari 2018). It has been shown that the increase in
plant growth and yield was not associated with the application of PSB by
increasing P uptake in plants (Poonguzhali et al. 2008). It is believed that PSMs, in
fact, have potential for controlling plant pathogens as well as plant growth
promotion through the production of siderophores, ACC deaminase, and IAA
(Han and Lee 2006; Sharma et al. 2013). As an example, Gulati et al. (2010)
reported that the phosphate-solubilizing strain BIHB723 belonging to
Acinetobacter was capable of producing other PGP metabolites such as IAA, ACC
deaminase, siderophore, and ammonia. In addition to solubilization of P in growth
medium (rhizosphere), P absorption by the plant depends on root growth. The root
system is especially important because it helps the plant to absorb water and
nutrients (Etesami and Alikhani 2016a; Fageria and Moreira 2011). The absorption
of P by plant is proportional to root density, so increasing rooting system increases
the plant’s ability to absorb P from soil (Grant et al. 2001). For example, Iqbal
Hussain et al. (2013) stated that increased P uptake by plant could be due to
increased root growth or root hair lengthening by specific microorganisms. It has
been reported that low amounts of IAA result in prolonged initial roots, while high
levels of IAA lead to an increase in the formation of lateral roots (Xie et al. 1996).
Also, keeping the concentration of ethylene in low amounts can increase root
growth. PSB with the ability to produce ACC deaminase can maintain the
concentration of ethylene in low amounts through the hydrolysis of ethylene to
ammonia and α-ketobutyrate (Pereira and Castro 2014). It seems that the
combination of these mechanisms in PSB has the most effect on increasing plant
growth indices under nutritional deficiency stress such as P (Etesami and
Maheshwari 2018).
It has been found that the establishment and performance of PSMs are affected
severely under environmental stresses including salinity (Johri et al. 1999). In
other words, the solubilization ability of phosphate by PSMs decreases in the
presence of salinity (decrease in the amount of inorganic P released by PSMs with
increase in NaCl concentration) (Cherif-Silini et al. 2013; Sánchez-Porro et al.
2009; Srinivasan et al. 2012). However, it has been reported that the
microorganisms (halotolerant microorganisms) isolated from saline environments
or halophytes were able to maintain their ability in solubilizing phosphate in the
presence of salinity (better performance of PSMs of salt-affected soils in releasing
inorganic P from TCP (tricalcium phosphate) under salt stress conditions)
(Etesami and Beattie 2018). It has been reported that PSB were also isolated from
the stressed environments (Chen 2006; Etesami and Beattie 2018; Etesami and
Maheshwari 2018). For example, the Kushneria sinocarni, a salt-loving strain,
were isolated from salt lake sediments on the east coast of China and showed
phosphate solubilization (Zhu et al. 2011). In another study, Srinivasan et al.
(2012) showed that the amount of inorganic P
released from TCP by the PSB strains (e.g., Aerococcus sp. strain PSBCRG1–1,
Pseudomonas aeruginosa strain PSBI3–1, Alteromonas sp. PSBCRG, etc.) was
found to increase with an increase in salt concentration up to 800 mM NaCl,
whereas the reference strain (P. striata) showed a significant decrease in P-
solubilization at NaCl concentrations. Phosphate-solubilizing salinity-resistant
bacteria (e.g., Klebsi- ella sp., Pseudomonas sp., P. stutzeri, Agrobacterium
tumefaciens, Ochrobactrum anthropi, Halomonas elongata, H. eurihalina, H.
sinaiensis, H. halmophila,
H. ilicicola, H. indalina, H. variabilis, H. xinjiangensis, H. taeheungii,
Zhihengliuella sp., Vibrio alginolyticus, Brevibacterium casei, Marinococcus
halophilus, Halobacillus trueperi, Nesterenkonia halobia, Oceanobacillus
picturae, Virgibacillus olivae, Chromohalobacter marismortui,
Haererehalobacter sp., Cronobacter sakazakii, and Chromohalobacter salexigens
(Jha et al. 2012; Mapelli et al. 2013; Sharma et al. 2016) were also isolated from
halophytes such as Arthrocnemum indicum, Salicornia strobilacea, and Salicornia
brachiate. These bacteria were also able to supply the plant P and thus the growth
of the plant under saline conditions. For example, following the inoculation of
Solanum lycopersicum plant with phosphate-solubilizing Achromobacter
piechaudii, the amount of plant P increased under salinity stress (Mayak et al.
2004a). In another study, the content of P in leaves of salinity-stressed wheat
inoculated with phosphate-solubilizing
B. aquimaris was significantly enhanced in a field experiment (Upadhyay and
Singh 2015). A screen of the mangrove Avicennia marina rhizosphere identified
129 bacterial strains with the ability to solubilize rock phosphate up to 97% (El-
Tarabily and Youssef 2010). Phosphate-solubilizing bacteria isolated from
halophytes (e.g., Arthrobacter, Bacillus, Azospirillum, Vibrio, Phyllobacterium,
and Oceanobacillus picturae) were able to solubilize Ca3(PO4)2, AlPO4, and
FePO4 (Banerjee et al. 2010; Bashan et al. 2000; El-Tarabily and Youssef 2010;
Yasmin and Bano 2011) and increase P content in both host plants and nonhost
plants (halophytes and glycophytes) under salinity stress. In addition, when the
oilseed halophyte Salicornia bigelovii was inoculated with phosphate-solubilizing
halotolerant bacteria (i.e., Vibrio, Azospirillum, Bacillus, and Phyllobacterium),
content of P in foliage also increased over non-inoculated plants (Bashan et al.
2000).
As mentioned above, in addition to bacteria, ability of solubilizing insoluble
phosphate compounds in fungi has been well proven, constituting about 0.1–0.5%
of total fungal populations (Kucey 1983). It is well known that the mycorrhizal
association increases host nutrient acquisition, particularly P (Smith and Read
2010). In one study, the effects of AM fungi Glomus intraradices and Gigaspora
margarita on Plantago lanceolata in poor soils showed that these fungi could
increase the absorption of nutrients such as N, P, and K, but the effectiveness of
each fungus was different (Veresoglou et al. 2011). The effect of mycorrhizal
fungi on increasing P absorption by plant is one of the most important effects of
these fungi. Mycorrhizal fungi extend beyond the root-depleted zone and play an
important role in exploring and extracting P outside the root-depleted zone. In
addition, other auxiliary mechanisms have been proposed for P uptake by
mycorrhizal fungi. Mycorrhizal hyphae have a lower Km than the roots of
plants. As a result, the minimum
concentration or threshold concentration for fungal hyphae fungi is lower than

roots of plant. Mycorrhizal hyphae have the ability to access microsites. These
fungi can access the inorganic and organic P forms that are inaccessible to non-
mycorrhizal plants (Zwetsloot et al. 2016). By secreting organic acids, which
mobilize inorganic P from rock phosphate and phosphatase enzymes, fungi such
as Aspergillus and Penicillium spp. and AM fungi belonging to the phylum
Glomeromycota Rhizophagus intraradices and Funneliformis mosseae (Krüger et
al. 2012) were able to increase the P availability and consequently enhance P
uptake in diverse crop plants (Barrow and Osuna 2002; Cozzolino et al. 2013;
Koide and Kabir 2000; Owen et al. 2015; Richardson and Simpson 2011; Smith et
al. 2011; Vassilev et al. 1996; Williams et al. 2013). These fungi can also increase
immobile nutrient absorption potential such as PO 43—, as a slowly diffusing ion, by
forming an extensive mycelial network within the soil (Owen et al. 2015) that
extends the plant’s effective absorption surfaces beyond the nutrient-depleted zone
that develops around the root caused by direct root uptake processes (Porcel et al.
2012). Fungal hyphae, which are functionally analogous to fine root hairs, also
support a microbial community (Andrade et al. 1998) with a high potential in
mineralizing and solubilizing recalcitrant nutrient complexes which are then
transported to the plant via the mycelial network (Owen et al. 2015; Toljander et
al. 2007).
Phosphate-solubilizing fungi have also been isolated from saline environments.
For an example, PSF such as Aspergillus sp. PSFNRH-2, isolated from salt-
affected soils, showed significant increase in P-solubilization with increase in
NaCl concentration up to 1.0 M than the reference strain irrespective of NaCl
concentrations (Srinivasan et al. 2012). According to previous studies (Al-Karaki
2000; Giri et al. 2003; Hirrel and Gerdemann 1980; Ojala et al. 1983; Pond et al.
1984; Poss et al. 1985), the improved growth of mycorrhizal plants was primarily
related to mycorrhiza-mediated enhancement of host plant P nutrition (as the most
important strategy of salinity stress tolerance in AM-colonized plants) in saline
conditions. It has been reported that AM fungus moderates the negative effects of
Na+ and Cl— on salinity-stressed plant by increasing the availability of P of the
plant (Pfetffer and Bloss 1988; Poss et al. 1985) and maintaining vacuolar
membrane integrity, which prevents these ions from interfering in growth
metabolic pathways (Cantrell and Linderman 2001) and facilitates
compartmentalization within vacuoles and selective ion intake (Rinaldelli and
Mancuso 1996). The above findings can be interpreted as evidence of the salinity-
resistant phosphate-solubilizing fungi and PGPR’s ability to solubilize insoluble P
compounds under salinity stress.
5.5 PGPR and AM Fungi-Mediated Increase of K

Potassium (K) is one of the essential macronutrients of plants and is the most
abundant nutrient in plants after N. This nutrient is considered as a key parameter
of soil fertility and plant growth as without adequate K, the plants will have poorly
developed roots, grow slowly, produce small seeds, and have lower yields (Parmar
and Sindhu 2013). Potassium plays a very important role in photosynthesis, cell
division and growth, protein production, quantity and quality of products, and
increased plant resistance to diseases and pests (Saber and Zanati 1984).
Potassium is also required to activate over 80 different enzymes responsible for
such plant and animal processes as energy metabolism, starch synthesis, nitrate
reduction, photosynthesis, and sugar degradation. Without adequate amounts of
K, water is lost from the cells, and the plant cells weaken and start to wilt.
Potassium-deficient plants will have poorly developed cell walls with lower levels
of stored protein and starch, and they become an easy meal for sucking insects and
an easy target for invasion by fungal spores (Meena et al. 2014, 2015).
More than 90% of K in the soil exists in the form of insoluble rocks and silicate
minerals (Etesami et al. 2017; Parmar and Sindhu 2013). Most of the K is unavail-
able for plant uptake. Muscovite, orthoclase, biotite, feldspar, illite, and mica are
of the most important minerals including K, and the major amounts of K are
present in the soil as a fixed form which is not directly taken up by plant. Plants
obtain K from K originated from the addition of chemical fertilizers and/or K
present in soil (Sparks and Huang 1985). Most soils have relatively high
amounts of total K, but their available K is relatively low. Potassium is present
in several forms in the soil, including mineral K (more than 90–98% of soil K),
non-exchangeable K (approximately 1–10% of soil K), exchangeable K, and
dissolved or solution K. Among different forms of K, its available (water-soluble
K) and exchangeable forms are available for the use of plants, and the rest of the
forms are almost non-available for the use of plants (Sparks and Huang 1985).
Plants absorb K mainly in the form of K+ and from the soil solution. The amount
of K of soil solution is very variable and is typically between 1 and 10 mg/kg. The
clay minerals contain a large amount of K, and often there is a positive correlation
between available K (water-soluble K) and the amount of clay minerals in the soil
(Sparks and Huang 1985). Non-exchangeable K plays a significant role in plant
nutrition under intensive cultivation conditions, especially in cases where
exchangeable K is less than the plant’s adequacy limit (Mc Lean and Watson
1985). When soluble and exchangeable K of the soil decreases to less than the
plant’s adequacy limit, non-exchangeable K can be released from the layers of
clay minerals (Tributh et al. 1987). The amount of K released in these
conditions is influenced by the amount and type of K-bearing minerals such as
muscovite, potassium feldspar, and vermiculite (Steffens and Sparks 1997).
Many studies have shown that the release of non-exchangeable form and
structural unavailable forms of K compounds in to soil solution can
significantly contribute to the amount of K absorbed by the plant (Snapp et al.
1995). In addition to imbalanced fertilizer application, the introduction of high-
yielding crop varieties/hybrids, and the progressive intensification of agriculture,
which deplete K reserve of soils at a faster rate (Parmar and Sindhu 2013), soil
salinity has also caused K deficiency to be one of the major constraints in crop
production. Sodium-induced K+ deficiency has been implicated in various crops
(Botella et al. 1997). It has been reported that salinity (Na+ ions) affects K
uptake by plant and prevents its absorption (Barea et al. 2005; Colla et al. 2008;
Rawal and Kuligod 2014) by interfering with various transporters (competing
with K for binding sites essential for various cellular functions) in the root plasma
membrane, K+-selective
ion channels (Wild 1988). Na+-induced decrease of K uptake has been attributed to
the competitive intracellular influx of both ions (Cerda et al. 1995). The greater
absorption of sodium by plant in saline soils leads to increasing Na +/K+ ratio in
plant, disrupting various metabolic processes such as protein synthesis in the
cytoplasm (Tester and Davenport 2003). As mentioned above, K has many roles
in plant metabolism such as activating a range of enzymes. The high levels of Na
or high Na/K ratios can not only substitute for K role in activating enzymes but
can also disrupt various enzymatic processes in the cytoplasm (Bhandal and Malik
1988). Therefore, maintenance of adequate levels of K + is essential for plant
survival in saline habitats (Botella et al. 1997). Providing K for salinity-stressed
plants can partly reduce the negative effects of sodium on the plants. The K
absorbed by the plants can influence the ionic balance of the cytoplasm or Na
efflux from plants (Bach Allen and Cunningham 1983).
There are several ways to increase K solubilization and release K from K-bearing
minerals, but the use of soil microorganisms can be a good complement to plant
nutrition due to its ease of use and low cost (Etesami et al. 2017). The ability of
roots of plants and microorganisms in the weathering of minerals and significant
alterations in mineralogy has been reported in the past (Etesami et al. 2017;
Nabiollahy et al. 2006). Biochemical processes that are involved in weathering of
minerals mainly occur in the presence of soil microorganisms and are affected by soil
microorganisms. Several studies have reported the effects of biological processes and
secreted materials of the roots of plants and microorganisms on weathering of
minerals in rhizosphere environment (Arocena et al. 2012; Wu et al. 2008).
Among the microorganisms of soil, AM fungi and bacteria are of great impor-
tance in terms of K availability to plants. It has been reported that some beneficial
soil bacteria including potassium-solubilizing bacteria (KSB) (i.e.,
Acidithiobacillus ferrooxidans, Enterobacter hormaechei, Arthrobacter sp.,
Pseudomonas spp.,
P. aeruginosa Paenibacillus sp., P. mucilaginosus, P. frequentans,
P. glucanolyticus, Aminobacter, Sphingomonas, Burkholderia, Bacillus
mucilaginosus, Bacillus edaphicus, and B. circulans) could solubilize the
insoluble K to soluble forms of K by various mechanisms including production of
organic acids (i.e., succinic, citric, gluconic, α-ketogluconic and oxalic, lactic,
propionic, glycolic, malonic, succinic, fumaric, and tartaric acids), which enhance
the chelation of cations (e.g., Si and Al) bound to K and help for acidolysis of
surrounding environment of microbes or directly dissolve rock K, and inorganic
acids, acidolysis, polysaccharides, complexolysis, chelation, polysaccharides, and
exchange reactions (Etesami et al. 2017; Meena et al. 2014; Parmar and Sindhu
2013; Uroz et al. 2009). Potasium-solubilizing bacteria also contribute directly to
the growth of plants directly by increasing the solubilization of insoluble K
compounds through increasing rooting system and improving symbiosis-
mutually beneficial relationships with host plant at different stages of growth
(Etesami et al. 2017). Johnston and Krauss (1998) showed that if the root density
in the soil is low, the concentration of K in the soil solution should be so high that
the root can easily absorb K. The PSB with production ability of IAA and ACC
deaminase can also increase plant access to K by increasing the root system of
plant under nutrient deficiency conditions (Etesami
et al. 2017). Previous studies have also shown that these bacteria could exert
beneficial effects on growth of crop plants (Badr et al. 2006; Basak and Biswas
2009, 2010; Han and Lee 2006; Nadeem et al. 2007; Sheng 2005; Sheng and He
2006). Nadeem et al. (2007) reported that plants inoculated with ACC deaminase-
producing bacteria had higher growth and higher K +/Na+ and chlorophyll than
non-inoculated plants in saline conditions. Mayak et al. (2004a) also reported that
the absorption of P and K in tomato shoot increased under salinity stress by
inoculation of Achromobacter piechaudii RV8.
In addition to KSB, mycorrhizal fungi can increase the plant growth and yield
and absorption of nutrients (i.e., K) by increasing the absorption surfaces of plant
roots (Meena et al. 2014). Fungi such as Funneliformis mosseae, Aspergillus
terreus,
A. niger, Penicillium sp., and Rhizoglomus intraradices can increase the K level in
soil solution through the release of H+, CO2 and the production of organic acids/
organic acid anions (e.g., citrate, malate, and oxalate), which solubilize K from
insoluble K-bearing minerals such as feldspar and potassium aluminum silicates
(Meena et al. 2014; Prajapati et al. 2012; Sangeeth et al. 2012; Sieverding et al.
2015; Wu et al. 2005). These fungi also influence K mobilization through mycelial
transport (Rashid et al. 2016). It has been reported that AM fungi can also provide
plants with K under salinity stress (Giri et al. 2007; Mohammad et al. 2003; Ojala
et al. 1983; Porcel et al. 2012). For example, Giri et al. (2007), Colla et al. (2008),
and Zuccarini and Okurowska (2008) showed that AM plants had a higher concen-
tration of K in root and shoot tissues than non-AM plants under salinity stress.
Higher K+ accumulation by AM plants may help in maintaining a high K+/Na+
ratio, thus preventing the disruption of various enzymatic processes and inhibition
of protein synthesis under salt stress conditions (Porcel et al. 2012). The above
studies show that application of K-solubilizing microorganisms as bio-fertilizer
for agriculture improvement can reduce the use of agrochemicals and support
eco-friendly crop production in salt-affected soils. At the present time, there is a
little information on salinity-resistant K-solubilizing microorganisms (KSMs). So,
it is required to evaluate salinity-resistant microorganisms isolated from
halophyte plants and saline environments in terms of solubilizing K-bearing
minerals in the future.
5.6 PGPR and AM Fungi-Mediated Increase of

Micronutrients Availability Under Salinity Stress
Most of the micronutrients are poorly available in saline-sodic soils, and plant
growth is highly depressed on such types of soils (Yousfi et al. 2007). Plant
growth on these soils is affected concurrently by salinity and micronutrients
deficiency.
Iron (Fe), as a micronutrient, is needed by all kind of living organisms. This
nutrient is a component of many enzymes which are involved in diverse
biochemical processes including respiration, photosynthesis, and N 2 fixation
(Kobayashi and Nishizawa 2012). Fe deficiency depressed nodule mass and
particularly leghemoglobin content, number of bacteroids, and nitrogenase activity
(Garcia et al. 2015; Tang et al. 1990). Fe predominantly exists in nature in
ferric (Fe3+)
form. Plants absorb iron as ferrous (Fe 2+) form, which is oxidized to Fe 3+, thereby
forming insoluble compounds and leaving a very low amount of iron for microbial
or plant assimilation (Ma 2005). In general, the availability of Fe is very low in
calcareous and saline-sodic soils throughout the world (Rabhi et al. 2007).
Microorganisms including PGPR can increase the availability of micronutrients
for plants through various mechanisms, such as soil pH reduction and the
production of chelating agents (Miransari 2013). PGPR can produce chelating
agents in iron deficiency conditions, which are called siderophores. Siderophores
are small, high- affinity Fe(III)-chelating compounds that can scavenge iron.
These iron-siderophore complexes can be easily accessible to plants (Kloepper et
al. 1980). The other theory about the supply of iron via siderophores is the ligand
exchange. The iron provided through bacterial siderophores can interact with plant
siderophores (phytosiderophores) in the reaction of ligand exchange, and
eventually iron is absorbed through phytosiderophores (Latour et al. 2009).
Siderophore-producing PGPR were able to fulfill iron requirement for normal
growth of iron-starved tomato plants (Grobelak and Hiller 2017; Pii et al. 2015;
Radzki et al. 2013; Scavino and Pedraza 2013). It is noteworthy that halotolerant
PGPR (e.g., Brachybacterium saurashtrense sp., Serratia marcescens,
Acinetobacter, Pseudomonas sp.,
P. stutzeri, P. putida, Microbacterium, Streptomyces sp., S. umbrinus,
S. griseoplanus, S. exfoliatus, S. avidinii, S. europaeiscabiei, Bacillus sp.,
B. cereus, B. pumilus, B. simplex, B. mycoides, Serratia plymuthica,
Microbacterium sp., M. oxydans, Rhodococcus sp., R. equi, R. erythropolis,
Micrococcus luteus, Nocardia sp., Agrobacterium tumefaciens, Zhihengliuella sp.,
Brachybacterium sp., Vibrio alginolyticus, Brevibacterium casei,
Cronobacter sakazakii,
P. pseudoalcaligenes, Haererehalobacter sp., and Halomonas sp.) isolated from
halophytes such as Salicornia brachiate, Aster tripolium L., and Prosopis
strombulifera had a significant ability to produce siderophore that may also be
used in saline soils (Etesami and Beattie 2018; Gontia et al. 2011; Jha et al. 2012;
Sgroy et al. 2009; Szymańska et al. 2016). The potential evaluation of
siderophore- producing salinity-resistant PGPR isolated from halophytes in terms
of increasing the availability of other micronutrients (e.g., Zn, Mn, Cu, etc.) is also
suggested for future research (Etesami and Beattie 2018).
It has been shown that some PGPR can increase the manganese (Mn)
availability for plant. For example, PGPR such as Bacillus, Pseudomonas, and
Geobacter can reduce Mn4+ to Mn2+, which is a metabolically useful form of Mn
for plants (Osorio Vega 2007). These bacteria affect the availability of Mn in soil
mainly due to their effect on plant growth and thus root secretion (Etesami and
Maheshwari 2018). Increasing root secretions caused by bacterial activity leads, in
turn, to supply of electron (through decomposition of carbohydrate compounds in
root exudates) and protons (through the proton-secretion system of root cells)
needed to reduce MnO2 to Mn2+. In addition, PGPR can produce different chelating
agents such as phenolic compounds and organic acids that form soluble complexes
with Mn, Fe, and other micronutrients, preventing the precipitation of these
micronutrients. The effects of soil microorganisms on the availability of Cu and Zn
in soil are directly affected by the production of various compounds such as
phenolic compounds and carboxylic acids or indirectly affected by plant growth
and as a result of root exudates (Iqbal et al. 2010).
The role of mycorrhizal fungi in increasing the absorption of nutrients is

important only in the ecosystems that have nutrient deficiency (Cardoso and
Kuyper 2006). Enhanced acquisition of Zn, Cu, and Fe by mycorrhizal plants has
been reported (Al-Karaki 2000; Al-Karaki and Clark 1998; Marschner and Dell
1994). The extensive mycelial system of the fungi can absorb nutrients such as N,
P, K, Zn, Cu, and Fe. The nutrients absorbed by the fungi are not exclusive to the
fungi, and some of them are transmitted to the plant (Cardoso and Kuyper 2006).
Clark and Zeto (1996) showed that the use of AM fungi increased the Fe
concentration in corn shoots. In addition, symbiosis of mycorrhiza increased Fe
concentration in the sorghum plant (Caris et al. 1998). Zn availability is limited
due to the low mobility and partial availability of this element in soil. Also, the
absorption surface is an important parameter that affects the bioavailability of Zn.
Therefore, increasing the absorption surface through colonization of arbuscular
mycorrhizal fungi may have a special importance on Zn uptake in comparison
with other plant nutrient elements (Hajiboland et al. 2009). Root colonization by
AM fungi increases Zn absorption in root length unit due to increased root
absorption surface caused by growth of fungal hyphae (Gao et al. 2007). In
general, the above studies show that salinity-resistant microorganisms can increase
the availability of micronutrients to salinity-stressed plants by the production of
organic acids and chelating agents, increasing the rooting system of the plant (i.e.,
by production of IAA and ACC deaminase) and thus increasing the root exudates
(Etesami et al. 2015a, b; Etesami and Maheshwari 2018).
5.7 Conclusions
Water and soil salinity is one of the most important agricultural problems in arid
and semiarid regions. Utilization of soil halotolerant microorganisms is one of the
strategies to deal with this stress. Since use of chemical fertilizers in salt-affected
soils increases the salinity of the soil twice, and the application of chemical
fertilizers is not common, or is carried out at the minimum, the use of halotolerant
PGP microorganisms can reduce some limitations in the production of crop plants
in saline soils. However, their application as bio-fertilizer in field conditions
requires more research. A better understanding on the interaction of halotolerant
bacteria and AM fungi when applied under field conditions is required. The
clarification of the mechanisms used by halotolerant PGP microorganisms in
improving the availability of micro- and macronutrients under salinity stress may
help in the development of innovative and cost-effective management practices for
improving the fertility and crop production capacity of salt-affected soils.
Acknowledgment We wish to thank the University of Tehran for providing the necessary
facilities and funds for this study.
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Bacterial Endophytes from Halophytes:
How Do They Help Plants to Alleviate Salt 6
Stress?
Ignacio D. Rodríguez-Llorente, Eloisa Pajuelo, Salvadora Navarro-

Torre, Jennifer Mesa-Marín, and Miguel A. Caviedes
Abstract
Soil salinization is one of the main factors influencing the reduction of crop
yield all over the world. Solutions for saline agriculture based on biological
systems involving plants or cultivars well-adapted to grow in soils affected by
salinity and associated microorganisms are gaining interest. Halophytes can
survive and reproduce in environments with high salt concentration and are
excellent models to study plant adaptation to saline environments. Plant growth
and adaptation, particularly in stress conditions, is highly influenced by
microorganisms that colonize rhizosphere and endosphere. Halophyte
microbiome has to be adapted to soil salinity and contribute to plant growth in
the presence of high concentrations of NaCl. Endophytic bacteria isolated from
halophytes growing in saline soils may help to alleviate plant by altering plant
hormone status and uptake of nutrient elements and/or modulating the
production of reactive oxygen species (ROS) through different mechanism,
including 1-aminocyclopropane-1-carboxylic acid (ACC)- deaminase activity,
phosphate solubilization, nitrogen fixation, and the production of indole-3-
acetic acid (IAA), abscisic acid (ABA), siderophores, and volatiles, among
others. In this chapter, the main genera of endophytes isolated from halophytes,
the presence of plant growth-promoting properties in these endophytes, and
how they could help to alleviate salt stress in plants are reviewed and discussed.
Keywords
Bacterial endophytes · Halophytes · Salt stress · PGPB
I. D. Rodríguez-Llorente (*) · E. Pajuelo · S. Navarro-Torre · J. Mesa-Marín · M. A. Caviedes

Departamento de Microbiología y Parasitología, Facultad de Farmacia, Universidad de Sevilla,
Sevilla, Spain

147
148 I. D. Rodríguez-Llorente et al.
6.1 Introduction
Soil salinization is a worldwide problem that could affect 1–10 billion hectares
with a potential increase of around 15% per year (Yensen and Biel 2006). It is
also estimated that up to 50% of the irrigated lands could be affected by
salinity or sodicity (Pitman and Lauchli 2002). This growing problem is one of the
main factors influencing the reduction in crop yields all over the world, since
salinity severely affects plant growth (Gerhardt et al. 2017). Revegetation and
remediation of ecosystems affected by salinity are mandatory to feed the world
growing population. Traditional systems to reduce soil salinity include lixiviation,
which requires high amounts of water, and the addition of organic and chemical
compounds, which are expensive and impoverish soils (Jesus et al. 2015). In that
way, biological systems involving plants and associated microorganisms are
gaining interest in salinity soil
remediation (Qin et al. 2016).
Physiological and molecular mechanisms undergoing salinity tolerance in
plants have been widely studied and reviewed (Deinlein et al. 2014; Gupta and
Huang 2014; Mickelbart et al. 2015; Zhu 2016). This information has been used to
develop strategies for alleviating crop salinity stress using plants (Ismail and Horie
2017). A group of these strategies is based on the construction of transgenic plants
overexpressing genes related with plant salt adaptation (Roy et al. 2014). Although
these approaches are still being developed, several aspects limit their success
including the following: (i) they require a lot of time and effort (Coleman-Derr
and Tringe 2014); (ii) the mutants sometimes are unstable (Jewell et al. 2010); (iii)
there are important tetraploid and hexaploid crop species for which molecular
techniques are not applicable (Kumar et al. 2015); and (iv) actually they do not
have a public acceptance, and this acceptance in the future is still uncertain
(Fedoroff et al. 2010). In addition, saline stress is frequently linked in nature to
other abiotic stresses, such as alkaline stress (Bui et al. 2014) or stress by organic
and metal contaminants.
Due to all these limitations, alternative ecological strategies involving plants or
cultivars well-adapted to grow in soils affected by salinity and microorganisms
associated with these plants are gaining interest to fight against soil salinization. In
this context, halophytes, plants that can survive and reproduce in environments
where the salt concentration exceeds 200 mM NaCl (Flowers and Colmer 2008),
are excellent models to study plant adaptation to saline environments and develop
strategies to improve salt stress tolerance in plants (Shabala 2013).
It is well-accepted that plant growth and adaptation, particularly in stress
conditions, is influenced by microorganisms that colonize plant rhizosphere and
endosphere, that is, the plant microbiome (Bhattacharyya and Jha 2012). Most of
these microorganisms have plant growth-promoting (PGP) properties, a group of
direct and indirect mechanisms that promote plant growth. Although it is not easy
to differentiate rhizospheric and endophytic microorganisms (most rhizobacteria
colonize the root surface and even penetrate into the root cortex), this chapter
will be focused on the mechanisms by which endophytes, particularly those
isolated from halophytes, could help plants to alleviate salt stress.
6 Bacterial Endophytes from Halophytes: How Do They Help Plants to Alleviate.. . 149
6.2 Halophytes and Their Associated Microorganisms
Comparing with human microbiome research, plant microbiome research is still

being born (Bai et al. 2015). Concerning halophyte microbiomes, only few have
been studied in the last decade, and most of them were works merely descriptive
that tried to classify and count microbial species (Ruppel et al. 2013). More
recently, microorganisms (particularly bacteria) have been isolated from the
rhizosphere of halophytes and screened for PGP properties and tolerance to NaCl.
Some examples are the isolation of plant growth-promoting bacteria (PGPB) from
the rhizospheres of Sesuvium verrucosum in Saudi Arabia (El-Awady et al. 2015),
Spartina maritima and Arthrocnemum macrostachyum in Spain (Mesa et al.
2015a; Navarro-Torre et al. 2016), or Salsola grandis in Turkey (Kataoka et al.
2017). There are also a lower number of examples of endophytes isolated from
halophytes such as Salicornia brachiata, Sphaeranthus indicus, Cressa cretica,
and Suaeda nudiflora growing in India (Arora et al. 2014); Halimione
portulacoides in Portugal (Fidalgo et al. 2016); or Spartina maritima and
Arthrocnemum macrostachyum in Spain (Mesa et al. 2015b; Navarro-Torre et al.
2016; Navarro-Torre et al. 2017a).
As expected, most of bacteria isolated from halophyte microbiomes were
halotolerant or halophiles, that is, they were able to grow at high concentrations of
NaCl or required NaCl to grow. How these microorganisms influence halophytes
adaptation to saline environments is an interesting unexplored task that is gaining
interest in the scientific community. The growing interest in these microbiomes
results in the recent isolation of a good amount of novel species with PGP
properties (Table 6.1).
Description of these new species most of the times requires sequencing their
complete genomes, providing good genomic resources to study the mechanisms
underlying plant growth promotion. In the same context, the study of the complete
microbiome of the halophyte Suaeda salsa revealed the presence of a high number
of genes contributing to salt stress acclimatization and nutrient solubilization
(Yuan et al. 2016). Halophyte microbiome has to be adapted to soil salinity, and
this advantage may be exploited to design bacterial bioinoculants for salt
phytoremediation or to sustain crop production in salty soils. In this sense, an
exhaustive revision on rhizobacteria isolated from halophytes and examples of
how they could help plants deal with salinity have been recently published
(Etesami and Beattie 2018).
6.3 Halophyte-Microbiome Interactions and Abiotic Stress
Halophytes have evolved to tolerate high salt concentrations employing several

well- described mechanism (Kumari et al. 2015a, b; Shabala 2013). These
mechanisms may be not exclusive to sodium and chloride and may confer
tolerance to other toxic ions and compounds. Indeed, some halophytes have
showed their ability to tolerate and/or accumulate high levels of toxic pollutants.
For example, several species of the genus Spartina are able to tolerate and
accumulate in their tissues organic and
Table 6.1 New bacteria species with PGP properties isolated from halophyte microbiomes in the
last 2 years
Halophyte New species Location Reference
Spartina maritima Marinomonas spartinae Endophyte Lucena et al. (2016)
Vibrio spartinae Endophyte Lucena et al. (2017)
Arthrocnemum Microbulbifer Rhizosphere Camacho et al.
macrostachyum rhizosphaerae (2016a)
Labrenzia salina Rhizosphere Camacho et al.
(2016b)
Vibrio palustris Endophyte Lucena et al. (2017)
Kocuria salina Rhizosphere Camacho et al.
(2017)
Halimione portulacoides Zunongwangia Endophyte Fidalgo et al.
endophytica (2017a)
Altererythrobacter Endophytes Fidalgo et al.
halimionae (2017b)
A. endophyticus
Saccharospirillum Endophyte Fidalgo et al.
correiae (2017c)
Plantago winteri Ancylobacter pratisalsi Rhizosphere Suarez et al. (2017)
Tamarix chinensis Salinicola tamaricis Endophyte Zhao et al. (2017)
Limonium sinense Glutamicibacter Endophyte Feng et al. (2017)
halophytocola
Anabasis elatior Aurantimonas Endophyte Liu et al. (2016)
endophytica
Suaeda maritime Martelella suaedae Endophyte Chung et al. (2016)
Limonium tetragonum Martelella limonii Endophyte Chung et al. (2016)
inorganic contaminants (Mackova et al. 2006; Redondo-Gómez et al. 2011).

Partic- ularly, S. densiflora and S. maritima were able to bioaccumulate high
levels of heavy metals in their tissues and mainly in roots (Redondo-Gómez
2013). In the same way, the ability of A. macrostachyum to accumulate high
amounts of Cd has been reported (Redondo-Gómez et al. 2010).
Microorganisms associated with halophytes could promote plant
phytoremediation capacity by reducing plant stress response (Mittler et al. 2004),
producing detoxification of pollutants, or acting over pollutant bioavailability.
Several recent works have reported the mitigation of toxic effects of pollutants on
halophytes by microorganisms of their microbiomes. For example, bacteria from
the rhizospheres of both Spartina densiflora and S. maritima were able to improve
plant growth under salt and metal stress (Mateos-Naranjo et al. 2015; Mesa et al.
2015c; Paredes-Páliz et al. 2017), and endophytes isolated from S. maritima also
improved plant growth in polluted marsh soils (Mesa et al. 2015b). Similarly, both
endophytic and rhizospheric bacteria associated with A. macrostachyum promoted
plant growth in heavy metal-contaminated marsh soils (Navarro-Torre et al.
2017b). Concerning organic pollutants, halophytes such as Juncus acutus,
Halocnemum strobilaceum, or
Scirpus triqueter assisted by their associated bacteria (both rhizospheric and endo-
phytic) have proven to be an interesting tool for hydrocarbon remediation in oil-
contaminated soils (Al-Mailem et al. 2010; Liu et al. 2011; Syranidou et al. 2017;
Zhao et al. 2013). Based on the results published in these works, the couple
halophyte-microbiome has been proposed as an ecological and efficient tool for
the restoration of contaminated and degraded marsh soils (Zhao et al. 2013).
6.4 How Do Endophytes Isolated from Halophytes Help Plants

to Alleviate Salt Stress?
Plant-associated microbes are essential for plant adaptation to salinity (Munns and
Gilliham 2015; Tkacz and Poole 2015). In general, the induction of plant tolerance
to different abiotic stresses is referred to as induced systemic tolerance (IST)
(Yang et al. 2009). PGPB elicit plant tolerance to salt stress (and other abiotic
stresses) by altering plant hormone status (Vurukonda et al. 2016) and uptake of
nutrient elements (Gerhardt et al. 2017) and/or modulate the production of reactive
oxygen species (ROS) (Gururani et al. 2013). Several bacterial traits seem to be
involved in these processes, including 1-aminocyclopropane-1-carboxylic acid
(ACC)-deaminase activity, phosphate solubilization, nitrogen fixation, and the
production of hormones, particularly indole-3-acetic acid (IAA) and abscisic acid
(ABA), siderophores, and volatiles (Fig. 6.1) (Farag et al. 2013; Kumari et al.
2015; Nadeem et al. 2016).
6.4.1 Endophytes and Plant Hormone Status
Plants subjected to salinity stress produce high levels of ethylene, which retard
root development (Mahajan and Tuteja 2005). Endophytes with the ability to
produce ACC deaminase, enzyme that catalyzes the conversion of the ethylene
precursor ACC to ammonia and α-ketobutyrate, could reduce plant ethylene levels
helping to overcome salt-induced growth inhibition (Senthilkumar et al. 2009). In
addition, these endophytes could provide a nitrogen source (ammonia) to plants
(Hardoim et al. 2008). ACC deaminase-producing endophytes have been isolated
from the halophytes
H. portulacoides, Limonium sinense, Prosopis strombulifera, S. maritima, or
Salicornia europaea, among others (Fidalgo et al. 2016; Mesa et al. 2015b; Qin
et al. 2014; Sgroy et al. 2009; Zhao et al. 2016). However, the direct effect of
these bacteria on plant growth under saline stress has been poorly explored. ACC
deaminase-producing endophytes isolated from L. sinense belonging to genera
Arthrobacter, Bacillus, Isoptericola, and Streptomyces showed the ability to
promote plant growth under salt stress (Qin et al. 2014). Interestingly, the most
promising strains showed no or very low levels of IAA and were not able to
solubilize phosphate, suggesting that the observed capacity to alleviate salt stress
may be related to their capacity to produce ACC deaminase (Qin et al. 2014).
Similarly, endophytes isolated from S. europaea that belonged to the genera
Arthrobacter, Bacillus, Planococcus, and Variovorax with ACC deaminase
activity enhanced in vitro seedlings growth in
Fig. 6.1 Overview of the mechanisms by which bacterial endophytes isolated from halophyte
microbiome could help to ameliorate plant growth in conditions of elevated salinity according to
published results. Endophytes can produce ACC deaminase and phytohormones to modulate
plant hormone status. ACC deaminase-producing endophytes reduce the excessive ethylene
production caused by salt stress. Endophytes are capable of increasing the antioxidative system
in plants for ROS scavenging. Endophytes can enhance plant nutrient uptake by several
mechanism and could accumulate or bind Na +. ABA abscisic acid, APx ascorbate peroxidase,
CAT catalase, GAs gibberellic acids, GPx guaiacol peroxidase, IAA índole-3-acetic acid, iWUE
water use efficiency, JA jasmonic acid, ROS reactive oxygen species, SA salicylic acid, SOD
superoxide dismutase, VOCs volatile organic compounds
the presence of increasing concentrations of NaCl; but these strains were also able
to solubilize phosphate and/or produce IAA, which could contribute to the
observed
S. europaea growth promotion (Zhao et al. 2016).
Secretion of phytohormones and particularly IAA in vitro is probably the most
common trait in PGPB (Duca et al. 2014). IAA is directly involved in root
generation and growth (Birnbaum 2016), so IAA-producing endophytes could
increase plant salt tolerance by stimulating root proliferation. IAA-secreting
endophytes have been isolated from several halophytes, including P.
strombulifera, A. macrostachyum,
S. maritima, S. europaea, H. portulacoides, or Psoralea corylifolia (Fidalgo et al.
2016; Mesa et al. 2015b; Zhao et al. 2016; Navarro-Torre et al. 2017a; Navarro-
Torre et al. 2017b; Sgroy et al. 2009; Sorty et al. 2016). IAA-producing
endophytes belonging to the genera Bacillus, Marinobacterium, and
Sinorhizobium isolated from P. corylifolia plants were able to enhance wheat
seedling growth under salinity stress when inoculated separately (Sorty et al.
2016). More recently, inoculation with an endophytic bacterial consortium isolated
from A. macrostachyum mitigated the
effects of high salinity on plant growth and physiological performance (Navarro-

Torre et al. 2017a). In that work, the bacterial consortium was composed of IAA-
producing endophytes from genera Bacillus and Gracilibacillus; nevertheless, the
increase in plant growth and salt tolerance cannot be directly attributed to the
production of IAA due to the presence in the endophytes of other PGP properties,
such as phosphate solubilization and siderophore production.
Modulation of plant abscisic acid (ABA), an important plant stress hormone, by
ABA-producing and/or ABA-metabolizing PGPB may also contribute to mitigate
the effects of salt stress in plants (Gerhardt et al. 2017). Nevertheless, the ability to
produce or metabolize ABA in endophytes isolated from halophytes has been
poorly investigated. Sgroy et al. (2009) reported the isolation of seven endophytic
bacterial strains from the halophyte P. strombulifera with capacity to produce
ABA in vitro. These strains belonged to the genera Achromobacter, Bacillus,
Brevibacterium, Lysinibacillus, and Pseudomonas. Most of these strains were also
able to produce gibberellic acids (GAs), a plant hormone that positively regulates
cell division and elongation, hypocotyl and stem growth, and leaf and root-
meristem size (Martínez et al. 2016; Wang et al. 2015). Although GA signaling is
a key factor in the inhibition of plant growth under stress (Martínez et al. 2016),
production of GAs by endophytes is not frequently assayed. Other hormones that
are also involved in abiotic stress resistance in plants, such as jasmonic and
salicylic acids (Ahmad et al. 2016), are also synthesized by several endophytes
(Chen et al. 2014; Forchetti et al. 2007), but their production by endophytes
isolated from halophytes has not been explored until date.
6.4.2 Endophytes and Plant Nutrient Uptake
PGPB can enhance the uptake of nutrients in plants. Endophytes with the ability to
solubilize insoluble phosphate, potassium, and zinc, fix atmospheric nitrogen
asymbiotically and/or release siderophores to scavenge iron which could promote
plant growth under abiotic stress (Santoyo et al. 2016). These bacterial traits are
often investigated in endophytes isolated from halophytes, but plant inoculation
with selected bacteria under saline stress is not so frequent (Sgroy et al. 2009).
Bacillus and Gracilibacillus endophytes isolated from A. macrostachyum showed
the ability to solubilize phosphate, fix atmospheric nitrogen, and produce
siderophores (Navarro-Torre et al. 2017a). A bacterial consortium containing three
of these endophytes was able to promote plant growth at high saline
concentrations and also to increase the level of NaCl accumulated by the plant
(Navarro-Torre et al. 2017a). Mesa et al. (2015b) also reported how a bacterial
endophytic consortium, including genera Micrococcus, Salinicola, and Vibrio,
helped to alleviate the effect of heavy metals and NaCl on S. maritima growth in
contaminated salt marsh soils. These endophytes combined in vitro IAA and
siderophore production, phosphate solubilization, and nitrogen fixation.
Interestingly, inoculation of S. maritima plants with the endophytes increased
(15%) water use efficiency (WUE), an important indicator of how plants manage
water under stress conditions (Tardieu 2012). Similar results were obtained using
an endophytic bacterial consortium isolated
from A. macrostachyum as inoculants (Navarro-Torre et al. 2017b). In this work,

endophytes belonging to genera Bacillus, Halomonas, Kushneria, and
Micrococcus ameliorated A. macrostachyum growth in salt marsh soils that were
also contaminated with heavy metals. This consortium was able to produce IAA
and siderophores, solubilize phosphate, and fix nitrogen asymbiotically.
6.4.3 Endophytes and Levels of Reactive Oxygen Species (ROS)
Increased production of ROS is commonly observed in plants growing under high

salinity (Miller et al. 2010). Endophytes may increase plant tolerance to salt and
other abiotic stresses modulating the production of ROS. An endophytic bacterial
consortium isolated from A. macrostachyum composed by genera Bacillus,
Halomonas, Kushneria, and Micrococcus induced changes in antioxidative
enzyme activities, such as ascorbate peroxidase (APx), catalase (CAT), guaiacol
peroxidase (GPx), and superoxide dismutase (SOD) (Navarro-Torre et al. 2017b).
These enzymes contribute to maintain the homeostasis against the high levels of
ROS (Mesnoua et al. 2016). A. macrostachyum plants inoculated with the
endophytic consortium showed enhanced APx, GPx, and SOD activities in saline
marsh soils contaminated with heavy metals, suggesting that endophytes could
contribute to reduce the oxidative stress derived from the amount of metal and
NaCl accumulated by the plant. Unfortunately, assays using endophytes and NaCl
as single abiotic stress are not found in the literature.
6.4.4 Endophytes and Other Mechanism of Salt Tolerance
Other mechanisms that could be relevant to PGPB-conferred salt tolerance have

been partially addressed using rhizobacteria. For example, inoculation with
rhizobacteria has shown upregulation of aquaporin gene expression (Gond et al.
2015; Qin et al. 2016; Vurukonda et al. 2016), directly related with root hydraulic
conductance that determines root water uptake capacity (Moshelion et al. 2015).
Some rhizospheric PGPB release volatile organic compounds (VOCs) that could
induce physiological changes in plants (Liu and Zhang 2015). Nevertheless, the
involvement of these mechanisms in plant salt tolerance elicited by endophytes
has not been explored until date.
Endophytes inhabiting halophytes have to be adapted to the salt concentrations
found within plant tissues. As previously indicated, most of the endophytes
isolated from halophytes mentioned in this review are halophilic or halotolerants.
These bacteria are able to grow in the presence of high concentrations of NaCl by
different mechanisms generally involving the synthesis or accumulation of organic
solutes to provide osmotic equilibrium of the cytoplasm with the surrounding
medium (Ventosa et al. 1998). Since halophilic and halotolerant bacteria are able
to accumulate Na+ within their cytoplasm or in the cell surface, it can be
speculated that sodium sequestration and/or accumulation by endophytes could
also contribute to plant tolerance and growth in saline environments.
6.5 Conclusion and Perspectives
Bacterial endophytes inhabiting halophytes have to be adapted to salinity and

contribute to plant adaptation and growth in salty soils. There are a growing
number of manuscripts describing the isolation and characterization of bacterial
endophytes from halophyte plants with PGP properties in vitro. Although
endophytic bacterial traits related with plant hormone regulation, nutrient uptake,
and ROS production, among others, might have a collaborative effect in eliciting
plant salt tolerance, direct demonstration of the concrete molecular mechanisms
involved in such induced tolerance has not been explored until date. Studies of
complete microbiomes of halophytes and comparison of recently sequenced
genomes of endophytes isolated from these plants could provide the genomic tools
to decipher the influence of the different PGP properties in plant tolerance. For
example, the construction of knockout mutants affected in the production of
concrete traits and the inoculation of plants with such mutants will help to
establish the influence of each trait or property in conferring salt tolerance. These
studies could provide useful information to select and design bioinoculants aimed
to improve crop production in salt-affected soils.
Acknowledgment We wish to thank the University of Sevilla for providing the necessary
facilities for this study.
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Effects of Halophilic Bacteria
on Biochemical Characteristics of Rice 7
Cultivars Under Salinity Stress Conditions
Mehvish Riaz Khattak, Sami Ullah Jan, Ijaz

Malook, Sehrish Riaz Khattak, Nazneen Akhtar,
Sehresh Khan, and Muhammad Jamil
Abstract
Soil salinization is a serious ecological problem affecting cereal crops including
rice. Different bacterial strains have been identified and used as salt remediator
in salt-affected soil, while there is confined use of halophilic bacteria. Present
study was aimed to find the growth stimulatory effects of two salt-resistant
Bacillus strains (NCCP-71 and NCCP-77) on biochemical changes in rice
cultivars (NIAB-IR-9 and KSK-282) under control (0 mM) and different salt
stress treatments (50, 100, and 150 Mm NaCl). High concentration of salinity
increased the Na+ ion content and lowered the K + and Ca+ ion contents in rice.
The rice seedlings inoculated with Bacillus strains showed a decrease in Na+
content followed by an increase in K + ion content. Calcium ions were increased
by NCCP-71 in both varieties; however NCCP-77 inoculation decreased
calcium ion content in KSK-282 and in NIAB-IR-9 at 50 mM NaCl. Salinity
gradually lowered the contents of photosynthetic pigments; however
inoculation with NCCP-71 and NCCP-77 caused a prominent increase in
photosynthetic content (Chl a, Chl b, and carotenoids) under salt stress. On the
other side, significant reduction in protein and nitrogen occurred with
increasing salt stress. Inoculation with bacterial strains NCCP-71 enhanced
protein and nitrogen content in both varieties, while inoculation with NCCP-77
enhanced nitrogen and protein content at 50 mM NaCl concentration. Both
halophilic bacteria had a great impact on the biochemical characteristics of
inoculated rice cultivar by modifying different biochemical processes under
saline conditions.
Keywords
Halophilic bacteria · Biochemical characteristics · Rice · Salt stress
M. R. Khattak · S. U. Jan · I. Malook · S. R. Khattak · N. Akhtar · S. Khan · M. Jamil (*)

Department of Biotechnology and Genetic Engineering, Kohat University of Science
and Technology, Kohat, Pakistan

161
162 M. R. Khattak et al.
7.1 Introduction
Plants are most susceptible to the climatic changes. The production of major crops
has been mainly affected by different stresses (Grover et al. 2011). Salinity is one
of the major obstacles to the agricultural practices today. The salt content in the
cultivated soil has been increasing due to irrigated water, desertification, and
extreme fertilization (Bacilio et al. 2004). Salinity affects the plants by inhibiting
cell division, elongation growth due to changes in homeostasis, ionic imbalance,
and osmotic potential (Principe et al. 2007). Salinity affects the physiological
parameters of plant growth by lowering the germination rate and percentage.
Abiotic stresses caused the alteration of growth parameters in plants (Kaymak et
al. 2009). Accumu- lation of toxic ions leads to reduced water uptake from the soil
and plants that rely on its carbohydrates to adjust its osmotic potential. This causes
reduction of the photosynthesis rate and closure of stomata (Yildirim et al. 2011).
Different techniques were streamlined by researchers in which most are using
sucrose (Siringam et al. 2012), phosphorus (Naheed et al. 2007), hormones
(Rafique et al. 2011; Afzal et al. 2006), priming with plant-derived smoke solution
(Jamil et al. 2013; Malook et al. 2014; Malook et al. 2017), and plant growth-
promoting rhizobacteria (PGPR) (Bhattacharyya and Jha 2012; Ashrafuzzaman et
al. 2009; Kaymak et al. 2008; Shah et al. 2017; Khan et al. 2017).
The free-living microbes that reside in plant roots and promote its germination
are called PGPR (Pallai 2005). PGPR uses two types of mechanism for increase of
growth by stimulating the maximum phosphorus uptake and solubilization,
biosynthesis and stimulating of plant growth hormones (indol acetic acid (IAA)
auxin, cytokinins and gibberellins), increased nitrogen and iron utilized by plants
roots through the production of iron rich siderophore etc (Mallesh 2008). Indirect
mechanisms involved the production of antibiotics against pathogenic bacterial
strains, biosynthesis of fungal cell disrupting enzymes, and formation of proline
content and glycine betaine which enhanced the overall systematic resistance to
pathogens and biotic stresses (Pallai 2005). Rhizobacteria are also termed as
biopesticides, biofertilizer, phytostimulator, and rhizomediators (Antoun and
Prévost 2005). Many bacterial strains were reported to have increases in plant
growth such as Pseudomonas, Azospirillum, Azotobacter, Enterobacter,
Klebsiella, Alcaligenes, Burkholderia, Arthrobacter, Serratia, Rhizobium, and
Bacillus (Saharan and Nehra 2011). Bacillus having a PGP activity especially has
resistant activity against plant pathogens. These bacteria form endospores and
have many beneficial compounds for agronomic purposes (Nihorimbere et al.
2010). Bacillus spp. increase plant growth by increasing beneficial compounds
such as butanediol and acetoin in a diverse of abiotic stress conditions including
salt and heavy metal stresses (Ryu et al. 2003). The most frequently PGPR
isolated from rhizosphere are of Bacillus spp. Research showed an increase in
yield of wheat by inoculation of Bacillus. Soybean seeds when inoculated with
Bacillus strains showed enhanced nodulation and growth (Gururani et al. 2013).
Soil salinization inhibits plant growth such as rice that is used as staple food.
Different techniques were used to minimize or remediate salt-affected soil, but
these
7 Effects of Halophilic Bacteria on Biochemical Characteristics of Rice.. . 163
methods are costly and also abolishing the soil structure and texture. Therefore,
different environment-friendly and economical methods have been utilized to
overcome this problem. Different bacterial species have been used to increase
the organic or inorganic contaminants in soils. The use of plant growth-promoting
bacterial strains isolated from rhizosphere has the potential to remediate soil
contamination. There is little information on the halophilic bacteria used for the
remediation of salt- affected soil. Therefore, the current study is to explore the role
of halophilic Bacillus strains (NCCP-71 and NCCP-77) on biochemical
characteristics of rice cultivars under different saline conditions.
7.2 Plant Materials
Rice cultivar seeds (cvs. NIAB-IR-9 and KSK-282) were obtained from the
National Agricultural Research Centre (NARC), Islamabad, Pakistan. Seeds were
sterilized with sodium hypochlorite solution 3.5% (v/v) and rinsed with distilled
water.
7.3 Bacterial Strains
Halophilic bacterial strains were taken from Plant and Microbial Biotechnology
lab, Kohat University of Science and Technology (KUST), Kohat, Pakistan,
already collected from Karak salt mines (Roohi et al. 2014). Halophilic bacterial
strains Bacillus spp. NCCP-71 and NCCP-77 were cultured according to Roohi et
al. (2012). The bacterial strains were grown at 37 ○C for 24 h with continuous
mixing in shaking growth incubator (Wise Cube, WIS-20R). Colony-forming unit
(CFU) was calculated to obtain 108 CFU/ml before inoculation of bacteria
according to the standard protocol of Rani and Arundhathi Reddy (2012) using
TSA agar supplemented with 5% (w/v) sodium content. The CFU was calculated
from the following equation:
Number of Colonies × Dilution Factor

Colony Forming Unit ¼ Volume of Inoculum
7.3.1 Sand Culture Experiment
The 10-day-old germinated seedlings of both varieties NIAB-IR-9 and KS-282

were transferred to plastic pots (having a hole in the bottom, covered with cloth)
containing about 1 kg of well-washed dried sand in the greenhouse. The seedlings
were sown 1 inch deep at a relative distance of a few cm apart from each other. All
the pots were germinated in Hoagland’s solution (Hoagland and Arnon 1950)
having pH of 5–6 and were allowed growing for 24 days.
7.3.2 Salt Stress and PGPR Treatment
After 24 days, stress of different salt concentrations 50, 100, and 150 mM NaCl
including control (0 mM NaCl) was given to plants mixed with Hoagland’s
solution for 1 week. To find the growth of halophilic strains Bacillus spp. NCCP-
71 and Bacillus spp. NCCP-77 under NaCl stress conditions, 10 ml of broth (10 8
CFU/ml) of each strain was also given along with Hoagland’s solution (Guo et al.
2011; Nabti et al. 2010). Fresh leaves randomly taken from three replicates were
crushed and placed at -40 ○C in Eppendorf tubes for molecular determination. The
rest of the materials was dried in an incubator at 80 ○C for 48 h and was powdered
for different biochemical tests.
7.3.3 Biochemical Parameters
7.3.3.1 Ion Analysis (Na+, K+, and Ca+2)

Ions were determined by using Flame Photometer (Jenway PFP7) according to the
standard protocol of Awan and Salim (1997). The plant material was oven-dried
and digested with to H 2SO4 and H2O2 at 2:1 (v/v) on a hot plate. The solution was
then diluted with 20 ml of distilled water, filtered with Whatman filter paper no.
41, and was processed for ion analysis.
7.3.3.2 Determination of Photosynthetic Pigments

Photosynthetic pigments (Chl a, Chl b, and carotenoids) were analyzed by taking
the 25 mg plant material along with 25 mg of MgO in 10 ml falcon tubes. The
mixture was supplemented with 5 ml of methanol and allowed to vortex at room
temperature. The homogenized mixture was kept on a shaker for 3 h at 250 rpm.
After that, all the samples were centrifuged for 7 min at 6000 rpm at ambient
temperature. All the plant extracts were noted on UV-visible spectrophotometer at
470, 653, and 666 nm using methanol as blank. The concentration of pigments
was calculated from the formulas mentioned by Lichtenthaler and Wellburn
(1985):
ðCa ¼ 15:65 A666 — 7:340
A653Þ ðCb ¼ 27:05 A653 —
11:21 A666Þ
ðCxþc ¼ 1000 A470 — 2:860 Ca — 129:2 Cb=245Þ
7.3.3.3 Nitrogen and Protein Content Determination

In digestion flasks, dried plant material was digested with H2SO4 at 400 ○C until
the solution becomes pale yellow. The mixture was diluted to 20 ml of distilled
water followed by the rapid drainage of 50% (w/v) of NaOH solution for 4 s. In
250 ml volumetric flask, 50 ml solution of 4% boric acid was taken with methyl
red as indicator. The distillation was terminated when the color of solution
changed into colorless. The mixture was titrated against 0.1 N H2SO4 and until
the pink color
Fig. 7.1 Effect of plant growth-promoting halophilic bacteria on (a) Na+, (b) K+, and (c) Ca+2 ion
contents of NIAB-IR-9 under different saline conditions
appeared (Peter and Young 1980). Total protein and organic nitrogen contents were
find by
. Σ
g Sample Volume — Blank Volume × 0:1N
Total Protein ¼ × 1:4007
g Dry Weight of Sample
. Σ
g Sample Volume — Blank Volume × 0:1N
Total Organic Nitrogen ¼ × 6:25
g Dry Weight of Sample
7.3.4 Results Ionic Content
The sodium ion content was increased with increase in salt concentration followed
by decrease in potassium and calcium ion concentrations in both varieties (Figs.
7.1 and 7.2). The inoculation of halophilic strains showed variations in ionic
contents of
Fig. 7.2 Effect of plant growth-promoting halophilic bacteria on (a) Na+, (b) K+, and (c) Ca+2 ion
contents of KSK-28 under different saline conditions
rice plants. The inoculation of plant samples with halophilic strains NCCP-71 and
NCCP-77 showed a decrease in Na + contents and an increase in K+ ion contents in
both varieties (Figs. 7.1 and 7.2). Calcium ion content was increased by
inoculation of NCCP-71 in both varieties (Figs. 7.1 and 7.2). NIAB-IR-9 showed
an increase in calcium ion content by NCCP-77 inoculation except at 100 mM
NaCl (Fig. 7.1c). KSK-282 showed a decrease in calcium ion contents by the
inoculation of NCCP-77 (Fig. 7.2c). This indicated that NCCP-71 has more
potential for stress alleviation.
7.3.5 Photosynthetic Pigments
Concentration of Chl a, Chl b, and carotenoids lowered under various salt

concentrations in both varieties (Figs. 7.3 and 7.4). The use of bacteria induced
significant changes in concentration of photosynthetic pigments (Chl a, Chl b,
Fig. 7.3 Effect of plant growth-promoting halophilic bacteria on photosyntetic pigments (a) Chl a,
(b) Chl b, and (c) carotenoid content of NIAB-IR-9 under different saline conditions
and carotenoids) in both rice varieties under saline conditions. The inoculation of
NCCP-71 led to an increase in pigment concentration in NIAB-IR-9 (Fig. 7.3a–c).
NCCP-77 inoculation showed an increase in Chl a and Chl b concentration at all
salt concentration except 150 mM NaCl in NIAB-IR-9 (Fig. 7.3). NCCP-77 had
no growth-promoting effect on carotenoid contents in NIAB-IR-9 (Fig. 7.3c).
KSK-282 showed an increase in concentration of Chl a, Chl b, and carotenoids in
control and 100 mM NaCl by inoculation of both strains NCCP-71 and NCCP-77
(Fig. 7.4).
Fig. 7.4 Effect of plant growth-promoting halophilic bacteria on photosyntetic pigments (a) Chl a,
(b) Chl b, and (c) carotenoid content of KSK-28 under different saline conditions
7.3.6 Total Organic Nitrogen and Protein Contents
Increase in salt concentration led to a decrease in protein and nitrogen contents

(Fig. 7.5). The inoculation of halophilic bacteria also induced changes in protein
and nitrogen content. NIAB-IR-9 plants inoculated with NCCP-71 had more
protein contents under all saline conditions. NCCP-77 inoculation increased
protein contents at 0 mM and 50 mM NaCl (Fig. 7.5a). The inoculation of both
strains increased nitrogen content under 0 mM and 100 mM NaCl concentration in
NIAB- IR-9 (Fig. 7.5b). NCCP-71 showed better results as compared to NCCP-
77. KSK-282 also showed a decrease in total organic nitrogen and protein contents
by increasing the concentration of salt (Fig. 7.6). KSK-282 plants inoculated with
NCCP-71 led to an increase in protein contents under all saline conditions. NCCP-
77 inoculation increased protein contents at 0 and 50 mM NaCl (Fig. 7.6a).
NCCP- 71-inoculated plants showed an increase in nitrogen contents under all
salt
Fig. 7.5 Effect of plant growth-promoting halophilic bacteria on protein (a) and total organic
nitrogen (b) content of NIAB-IR-9 under different saline conditions
concentrations. NCCP-77 inoculation increased nitrogen contents at 0 and 50 mM

NaCl (Fig. 7.6b). NCCP-71 yielded more increase in nitrogen and protein in
comparison to NCCP-77.
7.4 Discussion
Microbes isolated from rhizosphere has been widely used for the remediation of
inorganic metals, organic petroleum waste, and pesticides and for reclamation of
saline soils (Bose et al. 2008; Zeeb et al. 2006; Huang et al. 2004, 2005; Olson
et al. 2008; Lunney et al. 2004; Qadir et al. 2007; Su et al. 2008). Bacteria isolated
from salt habitat improve the effectiveness of the process. Therefore, the current
findings were aimed to assess the role of halophilic Bacillus strains (NCCP-71 and
Fig. 7.6 Effect of plant growth-promoting halophilic bacteria on protein (a) and total organic
nitrogen (b) content of KSK-28 under different saline conditions
NCCP-77) on biochemical characteristics of rice grown in salt-affected soil.

Increasing concentration of salt in soil increased Na + ions, while K+ and Ca+ ion
contents decreased in the plant under saline condition (Figs. 7.1 and 7.2). This
high concentration in Na+ and lower in K+ and Ca+2 content may be due to the
ionic pool available in direct contact to plant cells with the outer environment
under stress. Plants exposed to the high salt concentration induce ionic and
osmotic stress (Niu et al. 1995; Serrano et al. 1999; Zhu et al. 1998). It is also
known that the hydrophobic-electrostatic imbalance occurs at the cellular level.
The regulation in ionic concentration is primarily vital for optimal functions of
cellular enzymes which are very crucial in maintaining the cellular protein (Wyri
Jones and Pollard 1983). Wang et al. (2012)
reported high contents of sodium ions under saline stress condition as the NaCl
concentration increased. Similar results were reported by Jamil et al. (2012) who
studied the effect of salt stress on physiology and biochemistry of three rice
varieties including NIAB-IR-9. The inoculation of rice seedling with NCCP-71
and NCCP-77 reduced the sodium ions and increased the calcium and potassium
ions (Figs. 7.1 and 7.2). Both strains used were potent enough to reduce the Na+
concentration while they were able to keep the K+ and Ca+ concentration above the
untreated plants. Different research studies indicated that plant growth-promoting
bacteria inoculation reduced sodium ion content and increased potassium ion
content in plants (Nadeem et al. 2006; Zahir et al. 2009, Mishra et al. 2011;
Yildirim et al. 2011).
Photosynthetic pigments are very significant traits that link with photosynthetic
capability in rice (Teng et al. 2004). Photosynthetic pigments decreased with
increasing salt concentrations (Figs. 7.3 and 7.4). Salt stress decreased chlorophyll
a more than chlorophyll b (Figs. 7.3 and 7.4), as they are mostly affected by high
salts (Daiz et al. 2002; Santos 2004). The decreased ratio is the cause for lowering
the occurrence of photosynthetic contents in rice (Moradi and Ismail 2007; Zhen-
Hua et al. 2012). Inoculation with NCCP-71 significantly increased pigment
contents under saline conditions, while NCCP-77 increased pigment contents at
100 mM salt concentration in both varieties (Figs. 7.3 and 7.4). This increase in
contents may be due to important compounds such as butanediol and acetoin
formed by bacteria to increase the growth of a wide range of plants (Ryu et al.
2003). Priming with plant growth-promoting bacteria enhanced the pigment
content as reported by different studies (Zahir et al. 2009; Mishra et al. 2011;
Yildirim et al. 2011; Nadeem et al. 2006).
Increase in salt concentration also decreased the protein and nitrogen content
(Figs. 7.5 and 7.6). High salt content decreased the protein content and increased
the polyribosomes (Jones 1996). Lower concentration of protein content with
increase in NaCl was also reported by other studies (Khan 1998; Azooz et al.
2004; Dagar et al. 2004). PGPR inoculation led to an increase in organic nitrogen
and protein content (Nadeem et al. 2006; Mishra et al. 2011). In this study, protein
and nitrogen contents were enhanced in both varieties by NCCP-71 inoculation,
while NCCP-77 yielded enhanced nitrogen and protein content at 50 mM salt
concentration (Figs. 7.5 and 7.6). PGPR also stimulated increased nitrogen and
iron by plant which increased the protein contents in inoculated plants (Mallesh
2008).
7.5 Conclusion
The halophilic strains Bacillus spp. NCCP-71 and Bacillus spp. NCCP-77 isolated
from salt mines of Karak had an efficient ability to overcome salt stress by
inoculating with plant growth-promoting bacteria strains. These strains yielded an
increase in ionic contents, photosynthetic pigments, and nitrogen and protein
content. However, NCCP-77 showed sensitivity at some salt concentration.
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Production of Rhamnolipids by
a Halotolerant Bacterial Strain 8
with Seawater and Its Application
in the Treatment of Powdery Mildew
of Strawberry (Fragaria ananassa)
Xiangsheng Zhang and Boping Tang
Abstract
Biosurfactants are amphipathic compounds, a kind of natural agricultural chemi-
cal, excreted by microorganisms that exhibit surface activity. Biosurfactants
have advantages over their chemical counterparts in biodegradability, low
toxicity, and ecological acceptability and effectiveness at extreme
temperature and pH. Fermentation water and mineral salt costs are among the
production costs. The seawater is usually rich in various mineral salts.
Biosurfactant production with seawater and waste vegetable oil with simple
facilities will lower the cost greatly. In our study, strain screening, shaking
flask fermentation, and 5 L liquid fermentor fermentation were carried out
· fermentation yield reached above 10 g L —1, confirming
consequently, and the
this kind of low-cost production is feasible and practicable. And the application
of rhamnolipids in plant protection in saline soils was also conducted. · The
fermentation broth was diluted to 1 g L—1 and
0.5 g·L—1 separately and was directly used to treat the downy mildew of straw-
berry. The results showed that the fermentation broth could be used as an
efficient kind of fungicide. The pot experiments showed that control efficiency
could be reached over 90.8% and 87.6%, respectively, compared to blank
group, performing better than the tested dominant chemical fungicides.
Furthermore, the rhamnolipids fermentation broth could also enhance the
development of root and shoot of strawberry.
X. Zhang · B. Tang (*)

Jiangsu Key Laboratory for Bioresources of Saline Soil & Jiangsu Provincial Key Laboratory of
Coastal Wetland Bioresources and Environmental Protection, Yancheng Teachers University,
Yancheng, Jiangsu, China
Jiangsu Coastal Biological Agriculture Synthetic Innovation Center, Yancheng Teachers
University, Yancheng, Jiangsu, China

175
176 X. Zhang and B. Tang
Keywords
Seawater fermentation · Halotolerant biosurfactant producer · Rhamnolipids ·
Fungicide · Powdery mildew · Fragaria ananassa
8.1 Research Background
Biosurfactants are amphipathic compounds excreted by microorganisms that

exhibit surface activity (Zhang et al. 2012a, b). They have been found to be
produced mainly by aerobically growing microorganisms in aqueous media from a
carbon source feedstock, e.g., carbohydrates, hydrocarbons, oils, and other lipids
or mixtures thereof (Zhang et al. 2012b). Producers of surfactants include
Bacillus, Pseudomo- nas, Acinetobacter, Achromobacter, Arthrobacter,
Brevibacterium, Corynebacte- rium, Candida, and Rhodotorula (Pirog et al.
2012). Five major classes of biosurfactants are known, including glyco- and
phospholipids, lipopeptides, polymeric, and particulate surfactants (Shen et al.
2011; Zhang and Xiang 2010a).
Compared to the pure chemical surfactants, biosurfactants have many
advantages, such as being biodegradable, nontoxic, and eco-friendly and having
highly efficient surface activity, high tolerance to extreme environmental
conditions, and much lower critical micelle concentration (CMC) (Silva et al.
2017; Zhang and Xiang 2010a). Therefore, biosurfactants have been used in
microbial enhanced oil recovery (MEOR) (Bordoloi and Konwar 2008; Zhang and
Xiang 2010b; Zhao and Jiang 2004), petroleum chemical engineering,
environmental biological remediation (Li et al. 2000; Zhang 2013), agriculture,
cosmetic industry, food industry, etc. (Banat et al. 2000).
Glycolipids are among the most often bacterially produced biosurfactants
(Hatha et al. 2007; Zhang et al. 2012a), while the rhamnolipids are well-known
with many potential applications and are amidst the most widely studied
glycolipids (Henkel et al. 2012; Huang et al. 2009; Sodagari et al. 2017; Zhang
and Lu 2013). In this chapter, relevant fields of biosurfactants such as the
screening, fermentation, and application will be focused on rhamnolipid.
Furthermore, biosurfactants (in this paper, rhamnolipids) can be also used as
pesticides, bactericides, or fungicide. Ji Ye Ahn et al. once reported that one
isolate named SG3 could produce rhamnolipids, whose fermentation broth
inhibited mycelial growth of all of the tested fungal pathogens and effectively
suppressed the development of various plant diseases including rice blast, tomato
gray mold, tomato late blight, wheat leaf rust, barley powdery mildew, and red
pepper anthracnose. But presently other similar researches are not reported very
often.
The powdery mildew in strawberry (F. ananassa) in greenhouse often brings
about a huge loss in yield and qualities. In this study, an exploratory research on
fermentation of rhamnolipids by PW in laboratory scale and its application in
treatment of powdery mildew of strawberry in field scale was implemented with
the aim of clarification of the effectiveness of PW fermented rhamnolipids in the
treatment of powdery mildew in strawberry treatment.
8 Production of Rhamnolipids by a Halotolerant Bacterial Strain with.. . 177
8.2 Low-Cost Production of Biosurfactants
Theoretically, production of biosurfactants can carried out both by chemical

synthesis and microbial fermentation. But due to the complexity of
biosurfactants’ structures, the former production is very hard to implement.
Presently the fermentation method is the dominant one in biosurfactant
production, including living cell method, metabolically controlled cell method,
static cell method, and precursor addition method (Sarachat et al. 2010; Wu et al.
2007). Presently, free-living cell fermentation is the simplest and the most
common production method.
Although microbial biosurfactants have many advantages, their application in
abovementioned fields, especially in agriculture, was restrained due to the high
cost in production. So, lowering the production cost is among the research focuses
of microbiologists. The cost of the substrate will greatly influence the spread of
the biosurfactants. To date the low-cost production studies are mainly attracted by
using low-cost materials as carbon sources (Jain et al. 2013; Mukherjee et al.
2006), such as waste oil (Nitschke et al. 2005), slaughterhouse waste (Ramani et
al. 2012), distillery and curd whey wastes (Dubey and Juwarkar 2001), sugarcane
bagasse (Neto et al. 2009), potato process effluent (Noah et al. 2005), etc. It was
also reported that the production cost was also due to the severe foaming tendency
in aerobic fermentation and the relatively low productivity and yield. The
optimized fermentation produced 42 g L—1 rhamnolipids (Sodagari et al. 2017).
This might the highest yield once reported.
Waste oils such as thermally abused frying oils and oil phases accumulating in
communal sewage treatment plants are the most used carbon source to reduce the
production cost (Nitschke et al. 2005; Raza et al. 2006). They are largely not
recovered as a secondary resource, causing environmental pollution if disposed of
improperly or causing damage to public health if resold illegally as edible oils.
Waste oils, however, can be utilized to produce biosurfactants, such as
rhamnolipid used as emulsifier or demulsifier (Nitschke et al. 2005; Yao and Min
2010) as well as biodiesel (Xiong et al. 2007).
Although a mass of researches on halotolerant or halophilic biosurfactant
producers were carried out, production of biosurfactant from natural seawater
without or with adding mineral salt was rarely reported. The author of this chapter
put forward a new idea of fermentation with seawater to produce biosurfactants
(rhamnolipids) and put it into practices, achieving satisfactory results.
8.3 Screening of Biosurfactant Strains
Fermentation water and mineral salt costs are among the production costs. The
seawater is rich in various mineral salts, while presently seawater desalination is
expensive. Biosurfactant production with seawater and waste vegetable oil with
simple facilities will lower greatly the cost greatly. Fermentation with high salinity
(no lower than 30%) seawater is somewhat similar to fermentation under extreme
environments; then the screening of seawater-tolerant biosurfactant-producing
strains that can make use of seawater for fermentation is meaningful in coastal
areas. These strains also have a potential application in bioremediation of
hydrophobic contaminants in the sea. Usually screening of seawater fermentation
strains is the following (Miao et al. 2013; Zhang 2014):
8.3.1 Culture Media
High salt nutrient broth (NB) or seed medium was composed of, in g/L de-ionized
water, peptone 10, beef extract 5, and NaCl 35. For the preparation of nutrient
agar (NA) plates or slants, ·15.0 g L—1agar (strength 1300) was added. Blood NA
medium (3.5% NaCl) was all prepared as reference. Seawater fermentation broth
was composed of (g/L filtered seawater) yeast extract 1.0; pH was set as natural
value; 3% (V/V) frying oil (as the sole carbon source) was added to individual
shaking flasks. All the media were autoclaved at 121 ○C for 20 min.
8.3.2 Isolation and Screening of Halophilic Biosurfactant-

Producing Strains
About 5 g coastal soil samples or 5 mL seawater samples were aseptically added

to 45 mL sterilized seawater and streaked on blood NA plates. Colonies with big
and clear hemolytic circles were selected, incubated on slant media, incubated at
30 ○C, and stored at 4 ○C until further use. One loopful of culture was inoculated
in 20 mL of seed media in a 100 mL flask and incubated on a rotary shaker at 30
○
C and 180 rpm for 10 h. Then 2.5 mL (5%) inoculum was transferred to 50 mL
seawater fermentation broth in 250 mL shaking flask for 3 days. Then the broth
supernatant was centrifuged at 9000 rpm, and the biosurfactant-producing capacity
was measured. The strains that performed best were selected.
8.3.3 Measurement of Biosurfactant-Producing Capacity
In this section, all the protocols below are adopted as the author’s laboratory
conditions (Zhang et al. 2012b).
8.3.3.1 Oil-Spreading Method

About 30 mL distilled water was put into the Petri dishes (90 mm), and then 50 μL
diesel was dropped on the water surface to form an oil film, in the midst of which
5 uL fermentation broth, diluted by a factor of 10 with deionized water, was
dropped. The diameter of the oil expelling circles was measured by slide caliber
(with a degree of accuracy of 0.02 mm). The strains with big circle diameters were
selected for surface tension measurement. This method is usually used in
preliminary evaluation of fermentation broth surfactant production.
8.3.3.2 Surface Tension Measurement

The surface tension of the culture broth supernatant (diluted by a factor of 100)
was measured with a JYW-200 surface tension instrument.
8.3.3.3 Sulfuric Acid-Phenol Reaction Method

The fermentation broth was diluted by 100 times first, and 2 mL of the diluted
broth was transferred into a 15 mL glass test tube, 1 mL phenol and 5 mL sulfuric
acid was added and vortexed. Then the tubes were heated for 15 min in a boiled
water bath, cooled to room temperature, after which the optical density at 480 nm
was measured.
8.4 Fermentation Technology
In the laboratory level, there are three kinds of methods for free-cell fermentation:
shaking flask fermentation, small fermentor fermentation (liquid or solid), and
simplified fermentation. In shaking flasks, after 3 days fermentation, the waste oil
was emulsified obviously (Fig. 8.1). Using seawater media, the rhamnolipid
production was· 10.5 g L—1 in shaking flasks.
The appearance of fermentation broth in liquid fermentor was shown in Fig.
8.2, showing very good performance of seawater fermentation. The highest yield
could reach 33.0
· g L—1. With the fermentation process, the oil expelling circles
were increasing from 6.61 to 14.47 mm, while the surface tensions were
decreasing from · 78.9 mN m—1 to 36.2 N m—1. The 5 L fermentor fermentation
performed even better than shaking flasks, and this laid a solid foundation for
industrialization.
8.5 Application in Strawberry in Saline Soil
8.5.1 Treatment of Powdery Mildew of Strawberry
As shown in Fig. 8.3, the controlling effects of rhamnolipid fermentation broth

treatments were both better than the controls (A, mancozeb and B, triadimefon),
· 1 g L—1 and 0.5 g L—1 especially R1 treatment were
the control efficiency of
90.8% and 87.6%, increasing by 28.6% at most, and the difference was very
significant.
8.5.2 Effects on Root Development of Strawberry
As shown in Table 8.1, four treatments enhanced root development, the fresh root
weight, dry root weight, root length, root diameter, and root respiratory intensity,
especially rhamnolipids fermentation broth treatment, increasing over twofold.
Fig. 8.1 Fermentation by

seawater (left, no inoculum;
right, inoculated seawater
fermentation broth after
3 days incubation at 30 ○C)
Fig. 8.2 Rhamnolipid

production in 5 L liquid
fermentor
8.5.3 Effects on Shoot Development
As shown in Table 8.2, the shoot development was all enhanced after treatments.
The fresh shoot weight, dry shoot weight, average leaf area, and chlorophyll
content were all enhanced, especially R1 and R2, increasing by 10.8–48.2%.
8.6 Cost Evaluation
The cost evaluation is shown in Table 8.3.

It can be expected that the total cost of materials for fermentation broth is
very low.
100
**
90 **
80
Control effect(%)
70
60
50
40
R1 R0.5
A B CK0
Treatments
Fig. 8.3 Control efficiency of different treatments (R1, rhamnolipid fermentation broth 1.0 g·L—
1
; R2, rhamnolipid fermentation broth 0.5 g·L—1; A, mancozeb diluted by 800 times; B,
triadimefon diluted by 1000 times; CK0, deionized water; mm, means significant at P < 0.01)
Table 8.1 Effects on strawberry root development

Dry root Root Root
Fresh root weight length diameter Root respiratory intensity
Treatments weight (g) (g) (mm) (mm) (μmo1O2. min—1. g-1FW)
R1 10.52mm 2.95mm 352mm 0.65mm 0.83mm
R2 9.37mm 2.54mm 314mm 0.54m 0.70mm
A 6.86m 1.33m 229mm 0.46 0.60mm
B 6.27m 1.29m 201m 0.44 0.52mm
Control 4.84 1.18 162 0.42 0.23
Duncan’s analyses were used. R1, rhamnolipid fermentation broth 1.0 g ·L —1; R2, rhamnolipid
fermentation broth 0.5 g·L—1; A, mancozeb diluted by 800 times; B, triadimefon diluted by 1000
times; CK0, deionized water
msignificant at P < 0.05; mmsignificant at P < 0.01
8.6.1 The Principle of Fermentation by Seawater
The seawater is rich in mineral salts (Orban et al. 2007), although some
researchers found that cleaning up oil spills with the aid of microorganisms should
take into consideration the nutritional deficiencies of sea water (Atlas and Bartha
1972), that is, the seawater is deficient in nutritional elements for microorganisms
used for oil spill remediation. There are 11 kinds of the most abundant elements in
the seawater, including 5 kinds of cations: Na, Mg, Ca, K, and Sr (Li and Wu
1993). By
Table 8.2 Effects on shoot development

Fresh Dry
shoot shoot Chlorophyll
weight Increasing weight Increasing content Increasing
Treatments (g) by (%) (g) by (%) (mg. g-1FW) by (%)
R1 32.78mm 48.1 10.67mm 48.2 38.63m 16.4
R2 29.40mm 32.9 9.57mm 32.9 36.78m 10.8
A 25.54m 15.4 8.31m 15.4 35.32 6.4
B 24.47m 10.6 7.96 10.6 34.96 5.3
Control 22.13 0.0 7.2 0.0 33.2 0.0
Duncan’s analyses were used. R1, rhamnolipid fermentation broth 1.0 g L —1; R2, rhamnolipid
fermentation broth 0.5 g L—1; A, mancozeb diluted by 800 times; B, triadimefon diluted by 1000
times; CK0, deionized water
msignificant at P < 0.05; mmsignificant at P < 0.01
Table 8.3 Preliminary evaluation of cost only by fermentation materials

Materials Demand amount Price Total cost
1 t fermentation broth Seawater 1 t 0 0
Waste oil 30 L 1 USD·L—1 30 USD
Yeast extract 1 kg 5 USD·kg—1 5 USD
Sum 35 USD
comparison of seawater media fermentation and synthetic media fermentation, it

was found that NO3—, PO43—, and K+, as nitrogen, phosphorus, and potassium,
respectively, had great influence on fermentation yield. While too high
concentrations of Ca2+ and Mg2+ in seawater might suppress biosurfactant yield
(Liang et al. 2009). But in this study, fermentation by seawater showed good
results, the reasons were the follows: firstly, the other elements in the seawater
might compensate for negative effects of too high concentrations of Ca2+ and Mg2+
ions; secondly, the bacterial strains resisted high concentrations of cations.
Therefore, for the industrialization of fermentation by seawater, the screening of
optional strains is very important. There is only very limited nitrate-N in the
seawater (We et al. 2010). In this study, the concentration of nitrate-N in the
seawater was about 5 mg/L, much less than that in synthetic media; therefore, it
became one of limiting factors for seawater fermentation, and the research of
influence of adding nitrate or urea should be carried out for further improvement
of biosurfactant yield.
8.6.2 Potential Application of Seawater Fermented

Rhamnolipids in Agriculture
Biosurfactant has a strong commercial potential (Jamal et al. 2014), but its
application in different fields is limited by the production cost. These papers
mainly deal with the cost relevant problems of the application of biosurfactant by
two means. The first is lowering the fermentation cost. In this study, seawater was
employed to
take place of pure water, lowering the production cost greatly. Secondly, the direct
application in plant protection with fermentation broth also decreased the cost of
its application. In this paper, the treatment of powdery mildew of strawberry was
carried out, with the controlling effects over 87.57%, respectively, compared to
blank group, performing better than commonly used chemicals. Furthermore, the
rhamnolipid fermentation broth can also be found to stimulate the root and shoot
development of strawberry. Rhamnolipids are of great potential as a kind of
natural fungicide. As for the application of rhamnolipids in strawberry culture, it is
suggested that it should be used at the concentration of 0.5–1 g· L—1 every 7 days,
totally 2–3 times to achieve more stable controlling effects.
8.7 Conclusions
The author first proposed biosurfactant fermentation by halotolerant strain with

seawater adding a limited amount of yeast extract (growth factor) and sufficient
waste vegetable oil (as carbon source) using the natural mineral salts in the
seawater with a bacterial strain isolated from coastal soil, lowering the production
cost greatly, while the rhamnolipids yield was higher than fermentation yield with
oil-containing wastewater in other references (Liang et al. 2009). In summary, the
seawater can be used to ferment biosurfactants including rhamnolipids, and the
fermentation broth is effective at treating various plant pathogens, including
powdery mildew of strawberry. This study laid a foundation for further
application of wastewater fermentation broth in horticultural crop protection.
Acknowledgments This research was supported by the “333” Project of Jiangsu Province,
National Spark Program (2015GA690261), and Open Project of Jiangsu Provincial Key
Laboratory of Coastal Wetland Bioresources and Environmental Protection and Jiangsu Key
Laboratory for Bioresources of Saline Soil.
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Bottlenecks in Commercialization
and Future Prospects of Beneficial 9
Halotolerant Microorganisms for Saline
Soils
Bushra Tabassum, Adeyinka Olawale Samuel,

Muhammad Umar Bhatti, Neelam Fatima, Naila
Shahid, and Idrees Ahmad Nasir
Abstract
Salinity stress is a major abiotic stress that limits crop productivity. One way to
alleviate the effect of salinity stress on plants is to use salt-tolerant
microorganisms. Mechanisms employed by these salt-tolerant microbes not
only drive the plant to grow well in saline environment but also boost its
growth by producing various hormones, solubilizing phosphate, and fixing
nitrogen. Inconsistent field efficacy of salt-tolerant microbial formulations,
versatility for various crops, and economic aspects to develop such product by
industry are the bottlenecks in commercialization of these bioproducts. There is
no commercial formulation of salt-tolerant microbes currently available. For
sustained agriculture, formulations based on compatible halotolerant microbes
must be developed and marketed. This chapter focuses on the current status and
prospects of commercialization of microbial products based on halotolerant
microbes for increased crop production in saline soils.
Keywords
Halotolerant microorganisms · Saline soil-based agriculture · Bioproducts ·
PGPR · Biofertilizer
9.1 Introduction
Salt-dependent and salt-tolerant microbes with structural and metabolic

adaptations to thrive in various salt concentrations cut across Archaea, Bacteria,
and Eukarya domain. They can be categorized as extreme halophiles, moderate
halophiles, and halotolerant based on salt concentration requirement. Those that
survive within
B. Tabassum (*) · A. O. Samuel · M. U. Bhatti · N. Fatima · N. Shahid · I. A. Nasir

National Centre of Excellence in Molecular Biology, University of the Punjab, Lahore, Pakistan

187
188 B. Tabassum et al.
2.5–5.2 M salt concentration are referred to as extreme halophiles, while those that
fall within 0.5–2.5 M are moderate halophiles. The degree of salt accommodation
is similar in both except little change in some structural function. For instance, N-
glycosidically linked saccharides were found to differ significantly between
Halobacterium halobium (extreme halophiles) and Halobacterium volcanii
(moderate halophile) (Mengele and Sumper 1992). The stability of extreme
halophile Halobacterium halobium and Halobacterium salinarum in hypersaline
environment was attributed to the presence of di-acidic phospholipid,
archaetidylglycerol methylphosphate (PGP-Me) which prevent the leakage of cell
content (Tenchov et al. 2006). Several studies have focused on the adaptation of
halophile microbes to salt environment and the mechanisms employed (Paul et al.
2008; Argandona et al. 2010; Becker et al. 2014). Halophilic and halotolerant
microorganisms employed two basic osmoadaptation mechanisms to thrive in high
salt concentration environment which allow them to manage ionic strength and
water stress. In Salt-in- cytoplasm osmoadaptation mechanism, the salt
concentration in the cytoplasm is raised to a similar concentration as in the salty
environment, while during the organic osmolyte mechanism, the cell wall is
maintained by accumulation of uncharged, highly water-soluble, organic solutes
like sugars, polyols, and amino acids in response to an osmotic stress. These
nonionic, highly water-soluble compounds do not disturb the metabolism, even at
high salt concentrations. The effort in isolation and characterization of different
halophilics and halotolerant microorganism has led to their beneficial mining
toward the enhancement of salinity tolerance in crop plants.
9.2 Salinity Upsets Vegetative and Reproductive

Development in Crop Plants
A soil with electrical conductivity (EC) of the saturation extract (EC e) higher than
4 dS m—1 (approximately 40 mM NaCl) in the root zone and with exchangeable
sodium of about 15% is referred to as saline soil. Soil salinity deteriorates soil
quality and consequently reduces its agricultural potentials. The world continues
to lose hectares of farm soil daily to salt-induced degradation. Salinity upsets the
vegetative and reproductive development in crops. It inhibits plant growth either
by osmotic or ionic effects (Läuchli and Epstein 1990). The osmotic effect phase
constrains water uptake because in the saline soil solution, the osmotic pressure
lowers its potential energy. The ionic phase effects arise when specific ions
buildup over a period of time in the plant lead to ion toxicity or ion imbalance
(Munns and Tester 2008). High salinity reduces leaf expansion, stomata closure,
photosynthesis, and biomass loss due to water deficit caused by osmotic imbalance
(James et al. 2011; Rahnama et al. 2010). Most salt-tolerant plants have developed
osmotic adjustment mechanism that reduces the cellular osmotic potential by net
solute accumulation, which permits them to survive in salt-affected soil. Other
adaptive mechanisms include cell wall modification, reactive oxygen species
(ROS) detoxification, transport proteins, K+ and NO3—homeostasis, vacuolar
compartmentation, compatible solutes, etc.
9 Bottlenecks in Commercialization and Future Prospects of Beneficial.. . 189
Vacuole sequestration of Na+ detoxifies Na+ with the help of NHXs, while the
SOS signaling pathway exports Na + out of the cell. Studies have shown that the
NHX-type proteins are also important for compartmentalization of K+ into
vacuoles and for cellular pH homeostasis. The overexpression of AtNHX1 in
Arabidopsis was attributed to Na+ compartmentation in the vacuoles and has been
proven to improved salt tolerance Arabidopsis (Apse et al. 1999), tomato, and
canola (Zhang and Blumwald 2001; Zhang et al. 2001). Similarly ROS-
scavenging gene overexpressed in transgenic plant resulted in low cellular damage
and improved shoot and root growth in salt-affected soil (Roy et al. 2014).
9.3 Managing Salinity in Agricultural Land
Factors that contribute to the increasing salinity include weathering of primary

minerals and higher evapotranspiration rates, the increasing irrigation, excessive
fertilization, and processes of desertification (Ramadoss et al. 2013). Basically, salt-
affected soils are categorized as saline, sodic, and saline-alkali based on salt
accumulation. The salt- affected soils hamper crop yields and subsequently result in
huge economic damages. Saline-sodic fields effect on crops in the Indus basin in
Pakistan result to overall average loss of 32% in wheat and about 48% loss in rice
(Murtaza 2013). Khodarahmpour et al. (2012) reported 77.4% reduction in
germination percentage, 32.4% germination rate, and 95% seed vigor at 240 mM level
of salinity in maize.
Several methods have been employed for salt-affected soil mitigation toward
sustainable soil management and improved food production. However, attention is
given recently to microbial colonizing rhizosphere, bacteria, fungi, actinomycetes,
protozoa, and algae. But bacteria are the most abundant microbial present in the
rhizosphere. Specific halotolerant microbes are able to colonize the roots of plants
and enhance crop performance and plant growth in salt-affected soil. Rigorous
research has been carried out to identify the halophile strains that are suitable for
plant growth-promoting activities. Basically the following characteristics, nitrogen
fixation, phosphate solubilization, ACC (1-aminocyclopropane-1-carboxylate)
deaminase activity, and production of siderophores and phytohormones, are
usually investigated to confer the plant growth-promoting ability of specific
halophiles.
9.3.1 Biological Nitrogen Fixation
Biological nitrogen fixation (BNF) is the reduction of atmospheric nitrogen (N¼N)

to ammonia in the presence of nitrogenase complex that contains of two
metalloprotein components of the molybdenum-iron (MoFe) protein and iron
(Fe) protein (Hu and Ribbe 2015). Although BNF is a general activity in microor-
ganism, they are case of difference in mechanism mode. The N 2-fixing system of
non-heterocystous cyanobacteria contrasts from that of heterocystous
cyanobacteria significantly (Bergman et al. 2013). Nitrogenase activity of
cyanobacterium Trichodesmium was limited under aerobic conditions (Staal et
al. 2007). Unlike
other organisms BNF mechanism in halophile or halotolerant requires Na+.

Attempts have been made to establish whether Na + deficiency directly or indirectly
renders nitrogenase into inactive conformation and whether this can be reversed
by preincubation under acetylene (Apte and Thomas 1984). The loss of supply of
ATP in the absence of Na+ indicated that Na+ plays an important role in
maintaining supply of ATP to support various energy-linked functions, which
have also been observed in Pseudomonas stutzeri (Kodama and Taniguchi 1976,
1977). Several nitrogen fixation halophile bacteria that survive above 5% NACl
have been isolated and characterized (Zahran et al. 1995; Kang et al. 2015).
9.3.2 Phosphorus Solubilization
Phosphorus (P) is a very important element for plant growth, and a very little
amount is available for plant growth because it usually presents in insoluble form.
Recent research has shown that phosphate-solubilizing halotolerant plant growth-
promoting rhizobacteria (PGPR) enhance P availability to plants. Various
mechanisms like chelation, ion exchange, enzymolysis, and acidification by
secreting low molecular weight organic acids have been used to explain how
microbes solubilize insoluble phosphates and increase the available P for optimum
plant growth (Sharma et al. 2013; Etesami 2018). Srinivasan et al. (2012) isolated
several phosphate-solubilizing bacteria (PSB) and phosphate-solubilizing fungi
(PSF) from soil-affected soil. They reported that Aerococcus sp. strain PSBCRG1-
1 showed the maximum P-solubilization (12.12%) which was significantly
superior over all other isolates irrespective of NaCl concentrations, while
Aspergillus sp. strain PSFNRH- 2 (20.81%) recorded the maximum Pi release
irrespective of the NaCl concentrations and was significantly superior over all
other PSF.
9.3.3 ACC Deaminase Activity
Several microbes found in plant rhizosphere demonstrated the ability of ACC

deaminase production by the convection of the ethylene precursor (ACC) to α-
ketobutyrate and ammonium, reducing the ethylene levels in host plants and
making more nitrogen available for plant utilization. Enterobacter cloacae and
Pseudomonas sp. were found to produce and secrete large amounts of ACC
deaminase at about 10% salinity level NaCl (Trung et al. 2016). Similarly the
role of ACC deaminase from Ps. fluorescens strain TDK1 in alleviating saline
stress was evaluated in groundnut, and significant growth was reported in
groundnut inoculated with P. fluorescens strain TDK1 unlike other Pseudomonas
strains without ACC deaminase activity (Saravanakumar and Samiyappan 2007).
Recently the molecular interaction of ACC deaminase-producing endophytic
Streptomyces sp. GMKU 336 and its ACC deaminase-deficient mutant was
investigated. These bacterial strains were inoculated into Oryza sativa L. cv.
KDML105 under salt stress (150 mM NaCl) conditions. It was found that
Streptomyces sp. GMKU
336 significantly increased plant growth, chlorophyll, proline, K +, Ca+, and water
contents but decreased ethylene, ROS, Na+, and Na+/K+ ratio when compared to
plants not inoculated and those inoculated with the ACC deaminase-deficient
mutant. Furthermore, genes involved in the ethylene pathway, ACO1 and
EREBP1, were significantly downregulated (Jaemsaeng et al. 2018).
9.3.4 Production of Siderophores
Siderophores are low molecular weight iron-chelating compounds produced by

microorganisms (bacteria and fungi) to combat low iron stress and regulate its
uptake at various concentrations. They are categorized as catecholates,
hydroxamates, and hydroxycarboxylates based on their functional groups. Low
iron triggers a cascade of gene activation, allowing the cell to survive due to the
synthesis of important proteins involved in siderophore synthesis and transport
and release of chelates. Siderophores mobilize Fe and are effective at solubilizing
Fe for plant uptake and do not leach or decompose as readily as synthetic chelates
(Siebner-Freibach et al. 2004).
9.3.5 Phytohormones
Plant hormones or phytohormones are naturally organic substances which impact

physiological processes of plants at low concentrations. They affect differentiation
and development of plant growth via the regulation of diverse processes
(Tabassum et al. 2017). Plant hormones are categorized as auxins, gibberellins
(GA), cytokinins (CK), abscisic acid (ABA), and ethylene (Davies 2004; Jha et al.
2015). The increase in auxin (IAA) which caused a reduction of the uptake of
toxic ions by plants improved plant growth in high saline conditions (Chakraborty
et al. 2011). Two halotolerant strains of P. extremorientalis and P. chlororaphis
inoculated with Phaseolus vulgaris under high salinity conditions demonstrated
the impact of plant hormones like IAA, ABA, and GA3 on amelioration of salinity
stress in crop plant growth (Egamberdieva 2011). Similarly Ul-Hassan and Bano
(2014) reported an increase in the level of IAA and ABA in leaves of wheat grown
in saline soil upon inoculation with isolates of Pseudomonas sp. and Bacillus
cereus. A reduction in IAA concentration in leaves of soybean was reported after
48 h of inoculation while uninoculated plants showed an increase in IAA content
with salt stress (Asim et al. 2013).
9.4 Application of Halotolerant PGPR in Agriculture to Help

Plant Survive in Saline Environments
Halotolerant PGPRs are known to involve in array of agricultural-related

applications as detailed in Table 9.1 (Etesami and Beattie 2018), some of which
are outlined below:
Table 9.1 Summarized halotolerant strains and their particular role in plant growth promotion 19
NaCl Experimental 2
Halotolerant/halophilic bacteria Mode of action concentration plant Effects on plant References
Serratia sp. SL-12 – 150–200 mM Wheat Significant increase in plant Singh and
growth, as measured by Jha (2016)
parameters such as shoot/root
length, fresh/dry weight, and
photosynthetic pigment
accumulation
Pseudomonas fluorescens 002 Indole-3-acetic acid 150 mM Maize Increase in primary, lateral, and Zerrouk
(IAA) secretion and seminal root lengths and numbers, et al.
ACC-deaminase as well as root dry mass (2016)
activity
Klebsiella sp. SBP-8 – 150,175, and Maize Increased in plant biomass and Singh and
200 mM chlorophyll content. The bacterial Jha (2015)
strain caused Na+ exclusion (65%)
and increased uptake of K+
(84.21%)
in the host plant
Hartmannibacter diazotrophicus E19T ACC-deaminase 1%, 2%, and Barley Significant increase in root (308%) Suarez et al.
production 3% and shoot (189%) dry weight (2015)
Bacillus amyloliquefaciens NBRISN13 IAA and ACC 200 mM Rice Upgradation of Nautiyal
(SN13) deaminase NADPMe2, EREBP, SOSI, BADH et al.
production, and SERK1 and increase of (2013)
phosphate osmoprotectant
solubilization, and
proline accumulation B.
Bacillus amyloliquefaciens SQR9 Sequestering Na+ 100 mM Maize Upregulation of RBCS, RBCL, H+- Chen et al. Ta
into vacuoles, PPase, HKT1, NHX1, NHX2, (2016) ba
expelling Na+ from and NHX3 and significant ss
roots, accumulation promotion of the growth of maize u
m
et
9
of total solute sugar, seedlings and increase of the Bo
and enhancing chlorophyll ttl
antioxidant content Upregulation of the expression of en
genes related to salt tolerance and ec
downregulation of the expression ks
of genes related to ABA in plants in
Achromobacter piechaudii IAA and 172 mM Tomatoes Increase in the fresh and dry Mayak C
ACC-deaminase weights of tomato seedlings grown et al. o
activity (2004) m
m
P. fluorescens YsS6 and P. migulae 8R6 IAA and 165 and Tomatoes Increase of fresh and dry biomass, Ali et al.
er
ACC-deaminase 185 mM chlorophyll contents, and number (2014)
ci
activity of flowers and buds than the other
treatments ali
za
Azospirillum brasilense Nitrogen fixation 40, 80, or White clover Increase in plant growth under both Khalid tio
120 mM nonsaline and saline environments et al. n
(2017) an
Consortium containing strains Bacillus Phosphate 0, 510, and Arthrocnemum Mitigated the effects of high Navarro‐ d
alcalophilus EA1, B. thuringiensis EA3 solubilization and 1030 mM macrostachyum salinity on plant growth and Torre et al Fu
and Gracilibacillus saliphilus siderophores physiological performance (2017) tur
production e
Micrococcus yunnanensis, Planococcus ACC deaminase 50–125 mM Sugar beet Enhanced salt stress tolerance Zhou et al. Pr
rifietoensis, and Variovorax paradoxus remarkably in sugar beet, resulting (2017) os
in greater seed germination and pe
plant biomass, and higher ct
photosynthetic capacity s
Dietzia natronolimnaea STR1 Modulation of 50–150 mM Wheat Enhanced expression of TaST, a Bharti et al. of
ABA-signaling, SOS salt stress-induced gene (2016)
pathway, ion
transporters, and
antioxidant
machinery 19
(continued) 3
Table 9.1 (continued) 19
NaCl Experimental 4
Halotolerant/halophilic bacteria Mode of action concentration plant Effects on plant References
Klebsiella sp. strain Modulating 100 mM Oat Increase in physiological Sapre et al.
expression profile of parameter such as shoot length, (2018)
rbcL and WRKY1 root length, shoot dry weight, root
genes dry weight, and relative water
content (RWC) in inoculated plants
P. fluorescens ACC-deaminase 5% Cucumber Alleviated the negative impacts of Nadeem
activity, siderophore, salinity on plant growth et al.
and IAA production (2016)
Enterobacter sp. UPMR18 Antioxidant enzyme Okra Increase in germination Habib et al.
activities and percentage, growth parameters, (2016)
upregulation of ROS and chlorophyll content
pathway genes, and
ACC-deaminase
activity
Klebsiella, Pseudomonas, IAA and phosphate 1–20% Peanut A significant increase in total Sharma
Agrobacterium, and Ochrobactrum solubilization nitrogen (N) content (up to 76%) et al.
(2016)
Brachybacterium saurashtrense JG-06, Higher K+/Na+ ratio 100 mM Arachis Increase in plant length, shoot Shukla
Brevibacterium casei JG-08, and and higher IAA hypogaea length, root length, shoot dry et al.
Haererohalobacter JG-11 concentration, Ca2+, weight, root dry weight, and total (2012)
phosphorus, and biomass
nitrogen content
Bacillus licheniformis A2 IAA and phosphate 50 mM Peanut Increase in fresh biomass, total Goswami
solubilization length, and root length by 28%, et al. B.
24%, and 17%, respectively (2014) Ta
Bacillus endophyticus, B. IAA and phosphate 50–500 mM Glasswort Increase in plant growth under Zhao et al. ba
tequilensis, Planococcus solubilization saline stress conditions (2016) ss
rifietoensis, Variovorax paradoxus, u
and Arthrobacter agilis m
et
9
Bacillus sp. and Arthrobacter pascens Phosphate 100 mmol/L Maize Increase in accumulation of Ullah and Bo
solubilization and osmolytes, including sugar and Bano ttl
siderophore proline, and antioxidant enzymes (2015) en
production activity ec
Enterobacter asburiae, Moraxella ACC-deaminase 0.25 M Solanum Increase in seedlings fresh and dry Raheem ks
pluranimalium, and Pseudomonas activity lycopersicum biomass and Ali in
stutzeri (2015) C
Bacillus sp., Z. halotolerans, S. succinus, IAA production, 200 mM Triticum Increase in the root and shoot Orhan o
B. gibsonii, O. oncorhynchi, nitrogen fixation, aestivum length and total fresh weight of the (2016) m
Halomonas sp., and Thalassobacillus sp. and ACC-deaminase plant m
activity er
ci
Enterobacter sp. and Bacillus sp. ACC-deaminase 0 or 400 mM Chenopodium Improved plant water relations and Yang et al.
ali
activity, quinoa decreased Na+ uptake, which (2016)
za
exopolysaccharide consequently reduced osmotic and
tio
secretion, and IAA ionic stress
production n
an
d
Fu
tur
e
Pr
os
pe
ct
s
of
19
5
(i) Upregulate the activity of key enzymes, thereby activating plant antioxidant
defense machinery (Jha and Subramanian 2013; Islam et al. 2016; Qin et al.
2016);
(ii) fix atmospheric nitrogen by improvements in plant nutrition (Dodd and Perez-
Alfocea 2012; Etesami and Beattie 2017; Etesami 2018); (iii) maintain a high K +/
Na+ ratio, thereby enhancing the affectivity of inoculated plants (Giri et al. 2007;
Zuccarini and Okurowska 2008; Shukla et al. 2012; Islam et al. 2016; Etesami
2018); (iv) augment soil structure by promoting soil aggregation that is achieved
by exopolysaccharides (EPS)-producing-halotolerant PGPRs (Watanabe et al.
2003; Nunkaew et al. 2015); (v) help in altering root architecture and morphology,
hydraulic conductance, and hormonal status (Arora et al. 2006, 2012); and
(vi) enhance plant biomass and defense against drought stress, which are possible
due to emission of stress-related volatile compounds (Timmusk et al. 2014).
9.5 Stages of Commercialization
At present, no halotolerant formulation is available commercially. For

commercialization of halotolerant microbial product, several crucial steps are
required and are prerequisite starting from field survey, selection of microbes,
their compatibility with each other, geographical conditions in that particular area,
performance study of prepared formulation in laboratory conditions, and efficacy
testing in the field. Briefly, stages for commercialization of a halotolerant
consortium are underlined as:
9.5.1 Screening and Selection of Microbe
Availability and isolation of suitable microbes are trivial for commercialization of

a successful biocontrol/biostimulator product. This selection procedure ranges
from a specific environment and early trials to differentiate a microbe’s biocontrol/
biostimulator capability. Although no screening method can be singled out, a
plausible selection strategy could be followed based upon the pathosystem (plant-
pathogen-environment) of interest (Fravel 2005). This may include microbes that
colonize phyllosphere (Enya et al. 2007, Yoshida et al. 2012)/rhizosphere or the
ones that protect/promote a harvested crop (Janisiewicz and Korsten 2002).
Evaluation of suitable consortium of microbes is vital for selecting a potential
microbe. It is worth noting that even in the presence of highly efficient and robust
screening protocols, just less than 1% of candidate bacteria make efficacious
products (Bailey and Falk 2011). Thus, it is the need of the hour to come up hefty
microbial consortia to identify specific biocontrol/ biostimulator applicants. This
can be achieved via both target-directed and broad sampling techniques.
A simple model of microbial control/stimulator may consist of construction of
microbe databases. Such database would contain information on the isolates,
which could be aligned with required biocontrol/biostimulator compatibility,
pathogen targets, host plants, mode of action, and environmental niche, to name a
few (Glare et al. 2012). Every resulting subset can then be exposed to a chain of
standard
bioassays to establish biocontrol/biostimulator ability and on-field competence.

Importance of field setting as a marker of approval and application cannot be
neglected. It is common practice to establish biocontrol/biostimulator agents using
in vitro screening; however, a cautious approach should be taken while correlating
in vitro inhibition/promotion and field performance (Burr et al. 1996; Milus and
Rothrock 1997; Fravel 2005). There may be diverse screening strategies and
approaches, but they all should converge to form a microbial agent that is
effective, eco-friendly, and low on cost (Köhl et al. 2011; Ravensberg 2011).
9.5.2 Mass Production
To commercially produce such microbial agents, certain factors should be kept in

mind. First of all, a large (approx. 200 km 2), centralized location with better road
accessibility and unhindered electric supply is recommended. Secondly, one must
ensure uninterrupted supply of all the raw materials which may consist of mother
cultures, carrier materials (explained later), pet bottles, cardboard, and growth
materials. Thirdly, to set up a production facility of 250,000 l/year, almost 1 acre
of land is required. This land may be used to set up laboratory, installing tube
well, office, parking, and other facilities. The whole site must have a barbed wire
fence with suitable entry gates. Initially, 2000 m 2 of area can be covered for
regular operations.
A separate and closed biofertilizing unit must be constructed. This production
unit should be equipped with specific channels for microbial lab, production (fer-
mentation) area, packaging area, storage area, and marketing way. Latest and
efficient laboratory equipment, such as fermenters, culture medium tank,
fermenter assembly, autoclaves, boiler, broth dispensers for sterilization,
demineralizing plant, air compressor, etc., should be installed. All such equipment
should cater the overall production capacity. Steps for mass production of
halotolerant microbial suspension are shown in Fig. 9.1.
9.5.3 Preparation of Mother or Starter Cultures
Starter cultures of selected strains are obtained after determining their functioning
in greenhouse and at field levels. The pure culture of efficient strain of plant
growth- promoting organism is grown on respective agar medium and preserved
in the laboratory. This mother cultures are further reproduced in larger flasks.
After sterilization, each flask containing suitable broth is inoculated with the
mother culture in 1:5 proportions aseptically and grown in ideal conditions. This
broth culture with population of 109–1010 cells per ml should not be stored more
than 24 h or stored at 4 ○C. Fermenters are used for large-scale production of
microbial products.
For the production of liquid bioproduct, the broth from the fermenters directly
goes to the automatic filling machine and gets packed in, properly labeled, pet
bottles
Fig. 9.1 Steps for mass production of halotolerant microbial suspension
(varying volumes) as per the demand. The microbial count of the inoculants has to
be checked at the time of manufacturing. The viable cell count in the inoculants
should be maintained, for proper quality standards. The inoculants shall be stored
by the manufacture in a cool place away from direct heat. There are some quality
control standards for some microbial species, but there is no systemic certification.
There- fore, it is completely a voluntary monitoring system of quality checkup. It
is highly recommended that every unit should come up with proper arrangements
and measures for this purpose.
9.5.4 Carrier Material
Inoculations of biocontrol agents/biostimulator in seed or soil require carrier

materials. These materials are usually ground into powdered form with particle
size of 10–40 μm. A suitable carrier material is the one which (i) is inert and
nontoxic to inoculant bacterial strain, (ii) has fair moisture absorbance ability, (iii)
can be processed easily and does not contain lump-forming materials, (iv) can be
sterilized effortlessly by either autoclaving or gamma irradiation, (v) is available
in sizeable amounts, (vi) is cost-effective, (vii) has higher seed adhesion
capability, and (viii) can buffer the overall pH values. Above all, it must not be
toxic to plants. Peat, along with lignite, bentonite, and charcoal, is commonly used
as carrier material for seed inoculation. A lot of countries use rhizobial inoculant,
based on peat; information regarding its properties and effects is readily available.
For soil inoculation, carrier material in powdered or meshed form (0.5–1.5
mm) is generally used. Such granular forms of peat, perlite, charcoal, or soil
aggregates are appropriate for soil inoculation. Carrier selection with respect to
persistence of
inoculant bacteria depends on many different factors which include the following:
(i) once the seeds are coated with bacteria, they’re left to dry so that bacteria could
survive drying conditions. After drying, the coated seeds are then sown;
(ii) inoculant bacteria must also survive during the storage phase; and (iii)
inoculant bacteria should be well equipped to compete with natural soil microbiota
for nutrients and habitat. It must also save itself from grazing protozoans. This
survival trait requires microporous structure, which is found in soil aggregates and
charcoal. Therefore, such materials are automatic choices as carriers for soil
inoculant. After the carrier molecule is selected and before its usage, it undergoes
a rigorous sterilization. This ensures that higher number of bacteria remains
attached with carrier for longer duration of storage. Gamma irradiation is
considered best suited for carrier sterilization. Such technique does not alter
physical or chemical properties of the material. Another, most accessible and
commonly used technique is autoclaving. However, sometimes carriers undergo
changes in their properties and risk of the production of toxic substances for
certain bacterial strains.
Furthermore, studies have shown that aggregate-based inoculants that were
mixed with soil depict extremely enhanced survival as compared with those mixed
with soil without any particular carrier material. Also, such plants exhibited
significantly higher growth patterns in comparison with inoculants based on peat.
There- fore, it is highly recommended that soil aggregates might be appropriate
carrier materials for preparing cheap and effective, especially rhizobial, inoculants
(El-Fattah et al. 2013). Steps for selection of a suitable carrier material are shown
in Fig. 9.2.
For solid formulations, there is a requirement of lignite/bentonite/charcoal/peat
of desiredquality in powder form (70–100 mesh). However, the solid formulation
technology is gradually becoming obsolete because of the issues relating to the
quality and stability of the product. The solid-state formulation is sensitive to
Fig. 9.2 Steps for selection of a suitable carrier material and its desired characteristics for mass
production of halotolerant microbial suspension
temperature, and the microbial count comes below the threshold limit. In
comparison to the liquid formulation, it is a much stable technology, and the self-
life of the product can be maintained very well up to 12 months.
9.5.5 Laboratory Testing
The selected bacteria are first evaluated in pots in a control environment with
subsequent application in farmer fields. Extensive trials are done before the
product is to be marketed.
Although PGPR have the potential scope in commercialization, there are some
safety issues associated with environment and humans. The commercial
companies should therefore prefer the microbial consortia with zero impact on
human/environment health. The government should also regulate the screening
procedure and laws for selecting halotolerant strains for commercial purpose. The
safety concerns need to be clarified before the large-scale acceptance, registration,
and adoption of PGPR for pest and disease management.
9.6 Bottlenecks in Commercialization
As attention is recently drawn to the potentials of biofertilizer, farmers are not

aware of the opportunities and potentials of halotolerant PGPR to ameliorate soil
salinity. Even when they are aware, the acceptance level remains low because the
technology is still in infant stages and certain challenges must be overcome.
9.6.1 Characterization Challenges
A reasonable progress has been achieved in the identification of distinct halophiles

from other PGPR organisms. However, the most reported researches are still in the
basic stage unlike other halophiles. It is important to characterize potentially avail-
able halophile and evaluate their compatibility, because various mechanisms
involved in plant promotion may be host plant-specific and strain-specific.
Similarly the environment might affect the efficiency of the halophile in
promoting plant growth as impacts may vary under various environmental
conditions. Since the root rhizosphere contains several microbes, the identified
halophile must be a good competitor for nutrients and space for optimum
efficiency. Formulation of complex consortium of halophile or halotolerant with
effective plant growth across different saline region is paramount for the success
of commercialization.
9.6.2 Production Challenges
The lack in awareness could be as result of poor or low production of beneficial

halophiles. Although the same processes are involved in general production of
PGPR, the production on a large scale remains very challenging. Although the
setup cost of the producing plant is less expensive unlike chemical fertilizer, little
manufactories are recently available for its production. For the optimum utilization
of halophile microbes, it is penitent that the government should make an enabling
environment by promoting biofertilizer. Also establishing a sustainable policy,
which will boost the large-scale production of identified potential halophiles, will
increase crop production output in saline soil. More resource should be allocated
to improve on the level of awareness of the beneficial halophiles.
It must be noted that a successful microbial product is a result of multiple
factors (Ravensberg 2011). A study conducted by Gelernter and Lomer (2000)
suggests an outline for evaluating successful biocontrol/biostimulator products,
which enlist the following key properties of effective products:
(i) Efficacy of the product in laboratory, greenhouse, and field is a vital step to
achieve reproducible biological agent (Nicot et al. 2011; Whipps 2001).
Along with efficacy, the impact of mutation, viruses, and phase variation
should also be taken into account especially during industrial scale
manufacturing (Takors 2012). The effectiveness of the microbes in the
laboratory and in the greenhouse is not necessarily the same when applied
on the field level. The efficacy of data of the microbes in the lab lacks their
interaction with complex plant and soil environment, and thus, on-field
efficacy of the product also needs to be improved. Along with the on-field
effectiveness issue, there are other efficacy challenges involved, too, which
include the high-scale production of biological agents/biostimulator and their
extensive distribution in the field. Also, there is a question mark on the
genetic stability of the certain strains of bacteria for halotolerance because it
is very different to go from laboratory level to industry level.
(ii) Microbial strains should also effectively colonize the plants; their association
with roots is also an important step (Barea 2015; Compant et al. 2010). The
production of halotolerant bacteria, to be used as inoculum to improve plant
growth in saline soils, needs great care from the laboratory to the farm. It
also requires a proper study and assessment about the market it is going to
hit. The commercialization of every bioproduct to be used by the farmers
needs to pass several stages before getting approved. This includes the
selection of a certain strain of microorganism to be available for
commercialization. Also, that strain should have the activity that a particular
crop requires. Similarly, the weather conditions of certain area also affect the
activity of the bioproduct. The change in weather conditions results in
increased temperature which not only harms the plant but also influences the
activity of microbes by resulting in insufficient biological activity.
(iii) Plants use the microbes according to their needs, growth, and development
and the environment that they are growing in, along with the way they
respond to the biotic and abiotic stresses and the availability of the nutrients
in the soil. So, the effectiveness of any microbial strain inhabiting the plant
would be affected by all these factors. All these factors help the selection of
specific microbial strain for colonization for an adequate support to the plant
in meeting its functional needs. The microbial strains used as halotolerant in
increasing plant resistance to salinity in saline soils are required to have
consortia capable of adapting varying degree of salt concentration.
(iv) Practicality is another essential factor in the success of an inoculant.
Compati- bility of the product with production practices of farmers should
also be streamlined. The specificity related to crop of the microbial agents is
not dependent on their colonization in root. So, some strains can be, for a
certain crop, less specific, and for another crop, they can be much more
specific with the same concentration. Once the bacterial strains are colonized
in the roots, they produce certain metabolites which help the plant cope with
the issue they are dealing with by interacting with the plant. Thus, a
combination of microbes prepared for a certain crop as in sugar cane and is
showing a great activity, it would not be effective when it is applied on
another crop, for example, cotton. The reason could be the incapability of the
strains with the crop; also, the growth pattern of a certain crop can also
hinder the activity and survival of the biological agents.
(v) Products with extended shelf life and well protected against harsh conditions
are more sought after. Such formulations tend to enhance microbial life on
roots and leaves (Xavier et al. 2004; Warrior et al. 2002; Leggett et al. 2015;
Ravensberg 2011). For the faster commercialization of biological products,
their formulations need to be of broad spectrum, consistent in their action,
and with an increased shelf life. There are also some very serious factors
which need to be addressed for the development of a better biological agent
that include inoculant formulation, bulk level multiplication, selection of the
suitable strain, selection of the carrier, and marketing and packaging.
The proper formulation of microbial inoculant plays a critical role in the
stability of the microbial agent, its protection at the target site, increasing its
efficacy, and helping the delivery. One of the most important factors in the
race of decreasing the promotion of the inoculants is the development and
formulation of these biological products.
(vi) Persistence of microbial product in the field is a major issue (Chutia et al.
2007). Because these products have more specific targets, their shelf and
active life are usually less than chemical fertilizer/pesticides (van Lenteren
2012). Thus, the efficacy of a product presents a compromise between
immediate short-lived impact and persistence in the environment (Barea
2015).
(vii) Developing such biological control agents/biostimulator often require higher
costs, which hinder the success rate of these products (Dalpé and Monreal
2004). Therefore, production costs should align with investment returns and
economic aspect of such microbial products (Nicot et al. 2011).
Conclusively, effective utilization of halotolerant microbes for management of

saline soils will demand a rational choice of organism as well as technical
improvements in upscaling and formulation techniques. Genetic engineering of
plants expressing traits from halotolerant microbes may help crop plants survive
and withstand in saline environments. Therefore, a single bacterial strain with
multiple characteristics will facilitate plant to grow in saline environments and
simultaneously promote plant growth. It has become apparent that halotolerant
strains employ several mechanisms to promote plant growth, although studies
should be focused on the relative contribution of each mechanism responsible for
effective plant growth promotion. However, carefully controlled field trials of crop
plants inoculated with halotolerant inoculants are mandatory for maximum
commercial exploitation of these strains. In conclusion, the success of microbial
inoculant- producing industries will depend on measures including advanced
business management, product marketing, extensive education, and research.
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Role of Halotolerant Microbes in
Plant Growth Promotion Under Salt 10
Stress Conditions
Zahir Ahmad Zahir, Sajid Mahmood Nadeem,

Muhammad Yahya Khan, Rana Binyamin,
and Muhammad Rashid Waqas
Abstract
The salt-tolerant microorganisms also referred to as halotolerant including bacteria
and fungi have the ability to promote growth of plant in salty environment.
Presence of certain particular traits like exopolysaccharide production ability,
1-aminocyclopropane-1-carboxylate (ACC) deaminase, production of
osmolytes, enhancing nutrient acquisition and activity of antioxidant enzymes
as well as maintaining of K+:Na+ ratio make them suitable candidates for
promoting plant growth under saline environment. Moreover, the capability of
these microbes to fix nitrogen, produce siderophores, solubilize insoluble
nutrients, and provision protection against harmful pathogens further
accelerates the importance of beneficial microbes in agriculture system. To
make use of these environment friendly species as biofertilizers in agricultural
system is increasing nowaday to facilitate the plant growth under adverse
conditions. The halotolerant bacteria and fungi could be a cost-effective
approach to overcome the problem of salinity stress. These halotolerant
microbes can be used as biopesticides and biofertilizers and could decrease our
reliance on synthetic agrochemicals. These halotolerant microbes are also the
most suitable candidates for bioremediation of contaminated environment. This
review chapter highlights the significant role of halotolerant microbes for
improving crop growth under saline conditions and bioremediation of
contaminated environment. The mechanisms used by halotolerant microbes to
tolerate salinity as well as promote plant growth under salinity stress have been
discussed with selected examples. Also the role of these microbes in
environmental sciences has been reviewed. The areas that need further research
and future perspectives of this technology have also been discussed in detail.
Z. A. Zahir (*)
Institute of Soil & Environmental Sciences, University of Agriculture, Faisalabad, Pakistan
S. M. Nadeem · M. Y. Khan · R. Binyamin · M. R. Waqas
University of Agriculture, Faisalabad Sub-Campus Burewala-Vehari, Vehari, Pakistan

209
210 Z. A. Zahir et al.
Keywords
Halotolerant · Bacteria · Mycorrhizae · Stress · Plant · Growth · Environment
10.1 Halotolerant Microbes: An Introduction
In soil, plants face various environmental stresses including salinity, drought,

chilling, nutrient deficiency, pathogen, heavy metal, etc. Under stress
environment, plant faces a number of abnormalities in their growth due to
hormonal and nutritional imbalances, toxicity of a particular ion, and difficulty in
the uptake of water due to osmotic stress. All these factors result in poor plant
growth. Due to low rainfall and high temperature in arid and semiarid areas,
salinity is considered as a major environmental stress. Due to shortage of good-
quality canal water, the farmers have to use poor-quality underground water for
fulfilling the demand of irrigation. The quality of underground water in most of
the areas is not up to the mark, and the concentration of salts in soils increases due
to the recycling of poor-quality drainage water for irrigation (Shakirova et al.
2003).
To survive in saline environment, plants develop a number of physiological and
biochemical mechanisms including synthesis of osmolytes, ion compartmentaliza-
tion, activation of antioxidant enzyme, hormone modulation, ion exclusion, and
blocking the entry of sodium ion (Na+) into the cell (Tuteja 2007; Gupta and
Huang 2014). In addition to mechanisms used by the plant itself to tolerate
salinity, the microbial population occurring in the soil also plays a key role to
induce/enhance salinity tolerance in plants. Such microbial populations owing to
their number of growth-promoting traits and particular mechanisms cause a
significant positive impact on plant growth in harsh environment. Among these
microbial populations, certain bacterial and mycorrhizal fungal strains have the
capability to survive in saline environment. Such microbes are termed as
halotolerant and halophilic microbes. Halotolerance is the ability of living
organisms to maintain their growth under salinity, and these organisms can grow
under saline conditions, whereas halophiles live in highly saline environments and
require saline conditions for their proper growth. These microbes have evolved
particular characteristics that make them suitable candidate for their use in stress
agriculture as well as their use on commercial basis and in biotechnological
processes. These microbes also play significant role in cleaning contaminated
environment through their effective role in bioremediation processes.
Various halotolerant microbes including bacteria and fungi have the ability to
survive in saline conditions at variable concentration of salts. For example,
Staphy- lococcus epidermidis, Bacillus cereus, and Halomonas salina are
halotolerant bacteria that have the ability to survive up to 20% salt concentration
(Behera et al. 2012, 2014). Some of the well-known strains of halotolerant bacteria
include Bacillus aquimaris VITP4, Bacillus clausii I-52, Bacillus subtilis
RSKK96, and Bacillus licheniformis Shahed-07 (Joo and Chang 2005; Rasooli
et al. 2008; Shivan and
10 Role of Halotolerant Microbes in Plant Growth Promotion Under Salt Stress.. . 211
Jayaraman 2009; Akcan and Uyar 2011). Mandal (2014) reported that among
27 strains of Rhizobium trifolii, 5 strains were resistant to 3% salinity. Akhter
et al. (2012) while studying the salt tolerance mechanism of Azotobacter spp.
reported that out of 15 isolates, 5 were able to tolerate 6% NaCl and 2 strains
maintained their growth at 10% NaCl concentration. Prior to this, Tippannavar
et al. (1989) also reported the salinity tolerance ability of Azotobacter.
Halotolerant proteases have the ability to perform well at low as well as at high
concentration of salts. The capability of halotolerant bacteria to tolerate salinity
variable concentration of salts, i.e., 3–30% NaCl, makes them a suitable
candidate for their application in stress agriculture (Ventosa et al. 1998). Recently,
Banik et al. (2018) isolated halotolerant Bacillus and Halobacillus sp. from saline
environment. They reported that these bacteria also promoted groundnut growth in
saline as well as metal- contaminated conditions.
Similar to halotolerant bacteria, fungal species like Aureobasidum pullulans
and Wallemia ichthyophaga are considered as the most suitable organisms for
halotolerance studies (Gunde-Cimerman and Zalar 2014). Sengupta and
Chaudhuri (1990) and Hildebrandt et al. (2001) reported the presence of
mycorrhizal fungus in salt-marsh plants. Landwehr et al. (2002) also reported
about the occurrence of mycorrhizal spores in alkaline soils. Such salt-tolerant
fungi may be useful for improving crop growth under saline conditions. Manga et
al. (2017) while studying the impact of eight mycorrhizal fungi on the growth of
Acacia seyal under salt stress demonstrated that Rhizophagus intraradices
enhanced the growth of A. seyal at 680 mM NaCl by improving mineral uptake.
They further reported that presence of spores was independent of type of soil and
salts; however, degree of colonization varied among different mycorrhizal species.
Among different halotolerant fungi, Glomus spp. is the most commonly
occurring mycorrhizal fungus (Allen and Cunningham 1983; Wang et al. 2004).
Aliasgharzadeh et al. (2001) also reported that Glomus spp. were present in salt-
affected soils of Tabriz plains. They found the occurrence of G. etunicatum, G.
versiform, and G. intraradices in these soils having high ECe, i.e., 16 dS m—1. The
presence of Glomus sp. in the saline conditions has been reported by Wang et al.
(2004). The occurrence of these species in salty environment enables them to
facilitate plant growth by protecting them from negative impact of salinity. The
work of Porras-Soriano et al. (2009) also supported this concept, who tested the
plant
growth-promoting potential of three Glomus spp. (G. intraradices, G. mosseae, and
G. claroideum). They found that among these three species, G. mosseae was the
most efficient strain in terms of enhancing salinity tolerance of olive trees.
The salinity tolerance ability of same fungi may be varied with respect to their
stage of growth. As it has been seen in case of Glomus sp. that these strains
colonized the plant root in the presence of 300 mM NaCl, however, the spores of
this fungus did not grow at this salinity level (Juniper and Abbott 2006). They
demonstrated that it might be due to energy difference between different growth
stages as well as the critical limit of water and energy that is required to initiate
their germination.
The above discussion shows that a number of bacteria and mycorrhizal fungi
that have the capability to survive in salty environment. These species not only
maintain
their growth in saline condition but are also helpful to lighten the impact of stress
conditions on plant growth and development. The mechanisms used by these
microbes to tolerate saline conditions and promote the plant growth by reducing
the salinity impact are discussed in the next section.
10.2 Mechanisms of Salinity Tolerance in Halotolerant Microbes
In order to promote growth of plant under stress, the microbes must have the
capacity to sustain their growth in such harsh environment. There are a number of
mechanisms used by halotolerant microbes (bacteria and mycorrhizal fungus) to
tolerate saline environment and promote plant growth. The adaptation of these
microbes to saline conditions and then improving plant growth are related to their
particular traits and some specified mechanisms which provide them competitive
advantage over other soil microbial population.
Kunte (2012) while studying the mechanisms of osmoadoptation demonstrated
that halophiles use two basic mechanisms to cope with salinity. These mechanisms
include salt-in-cytoplasm and the organic-osmolyte mechanism. According to their
view, these mechanisms enable the halophilic microbes to flourish in saline
environment even in the presence of salt solutions with varying levels of salt
concentration. In salt-in-cytoplasm mechanism, the cytoplasm of halophilic
organism remains free from sodium (Na+), and they accumulate potassium ion
(K+) in their cell. The accumulation of potassium results in exposure of cytoplasm
to an increased ionic strength. In case of organic-osmolyte mechanism, the
bacteria accumulate organic solutes like sugars, polyols, and amino acids. These
nonionic solutes don’t disturb the metabolism even at high concentration.
According to them, compared to halophiles, microbes which are using salt-in-
cytoplasm mechanism, the organisms using organic-osmolyte mechanism are
more flexible because they can grow at high and low salt concentration. However,
organic-osmolyte mechanism requires more ATP compared to salt-in-mechanism.
To survive in stress environment, the halophilic bacteria accumulate compatible
solutes like glycine, betaine, proline, ectoine, and glutamate, whereas
accumulation of glycerol is well known in most of the fungi (Blomberg and Adler
1992; Burg et al. 2007). Many bacteria and a number of eukaryotic organisms
accumulate compatible solutes to maintain intracellular Na + concentrations below
the toxic levels. In halotolerant bacteria, in order to maintain osmotic balance due
to low intracellular salt concentration, they accumulate various organic solutes in
cytoplasm. These solutes keep away the cells from plasmolysis in the presence of
salty environment (Kempf and Bremer 1998). In heterotrophic eubacteria, ectoine
is the most abundant osmolytes (Galinski 1995) that was discovered in halophilic
Ectothiorhodospira halochloris (Galinski et al. 1985). In addition to glycine and
betaine, trehalose also plays a key part in organisms to tolerate stress tolerance
(Turan et al. 2012).
According to Mendpara et al. (2013) among six bacterial spp. isolated from
agricultural soil, two species Exiguobacterium sp.and Serratia sp.showed salt
tolerance up to 10% NaCl. They demonstrated that high salt tolerance ability of
these isolates might be due to the synthesis of betaine, ectoine, and trehalose as
reported by earlier workers (Oren 2008; Kondepudi and Chandra 2011). Recently,
Patel et al. (2018) studied the mechanism used by halotolerant Exiguobacterium
profundum PHM11to tolerate salt condition. They reported that this strain
accumulates L-proline to tolerate salinity. They further reported that salinity-
tolerant ability of this strain was also related to fine-tuning gene expression
profiles of related metabolic pathways. They observed that maximum growth,
biomass, and metabolite production occurred at 100 mM salinity and minimum at
1500 mM. Exiguobacterium sp. has already been reported to be present in cold
and hot environments with temperature
range from — 12 to55 ○C (Vishnivetskaya et al. 2009).
Osmotolerance strategy of Colwellia psychrerythraea 34H and Psychrobacter
sp. 7E was studied by Firth et al. (2016). They used 14C-choline (precursor to
glycine, betaine) and observed that this compatible solute allowed bacteria to
survive in variable salt conditions, i.e., short-term, long-term, or abrupt change in
salinity. They demonstrated that choline contained nitrogen and when bacteria
respired, the regeneration of ammonium might enhance specific biogeochemical
process possibly algal productivity but particularly nitrification.
One of the mechanisms used by the bacteria to survive under salinity is the
accumulation of potassium. The K+ ion accumulation in the cytoplasm of
halotolerant microbes is coupled with glutamate that is accumulated as a
counterion. This accumulation of K+ ions with glutamate has been reported in
Escherichia coli and other bacteria as well (Oren 1999; Ventosa et al. 1998;
Dinnbier et al. 1988). Similarly, tolerance of up to 11% salinity concentration by
the bacterial strains has been mentioned by Amir et al. (1993). They noted the
accumulation of sodium ions inside the cell, and to maintain intracellular balance
of sodium ions, bacteria accumulated K + ion and osmolytes like proline. However,
accumulation of high K+ may disturb the normal functioning of cellular enzymes,
and to solve this problem, bacteria use another strategy that is the accumulation of
compatible solute (Lucht and Bremer 1994; Galinski 1995; Ventosa et al. 1998;
Saum and Muller 2007).
Sandhya and Ali (2015) reported that halotolerant bacteria can survive under
harsh environment by synthesizing specific metabolites. The function of PDH45
(pea DNA helicase 45) in salt tolerance of various crops is well documented by
various reasercher (Sanan-Mishra et al. 2005; Sahoo et al. 2012; Augustine et al.
2015). However, its role in bacterial salt tolerance has been studied by Tajrishi
et al. (2011). They documented that salinity tolerance ability of Escherichia coli
BL21 was due to functionally active PDH45 gene. They also observed that stress
response is specific one, because bacteria could not grow when NaCl was replaced
with LiCl. It means this gene is specific for Na + and enhanced bacterial stress in
salinity caused by Na+.
The accumulation of proline, glycine, glutamate, and trehalose was also
observed in salinity-tolerant strain of Azospirillum brasilense (Tripathi et al.
2002). They demonstrated that proline plays significant role in bacterial
osmotolerance. They found that with increase in osmotic stress, the accumulation
of osmolytes shifts from
glutamate to proline. The ability of Chromohalobacter salexigens to tolerate

salinity was studied by Reina-Bueno et al. (2012) with respect to the role of
trehalose in this regard. They observed that the said mutant strain was not affected
by salinity when it was deficient in trehalose-6-phosphate synthase gene; however,
its double mutant deficient of ectoine and trehalose showed sensitivity to salinity.
They reported that trehalose plays a role in bacterial salinity tolerance. In addition
to help in osmoadaptation, compatible solutes also played an important role in
the protection of macromolecules, tissues, cells, and organs (da Costa et al. 1998;
Welsh 2000a, b).
Tiquia et al. (2007) isolated 127 halophilic bacterial strains that belonged to
genera including Staphylococcus, Bacillus, Paenabacillus, Halobacillus, Clostrid-
ium, and Halomonas. They found that most of these strains were positive for
gelatinase, β-galactosidase, and tryptophane deaminase enzymes. They observed
that arginine dihydrolase was the primary enzyme found in these isolates, and
according to their view, these enzymes were present in halotolerant bacteria that
helped them to survive in salty conditions. Upadhyay et al. (2012) studied the
salinity tolerance ability of the bacterial strains and reported that among about
33% isolates that were able to survive at 8% NaCl, only 19% showed plant growth
promoting traits at higher NaCl concentration. They studied the mechanism of
osmotolerance in bacteria and found that high concentration of proline and protein
was present in salt-tolerant strains.
Similar to bacteria, certain fungal strains can also tolerate saline conditions.
Similar to bacteria these strains also adopt various mechanisms that enable them to
survive in salty environment. Petrovic et al. (2002) mentioned that glycerol is one
of the most important compatible solutes that played an important role in salinity
tolerance of Hortaea werneckii. According to Plemenitas et al. (2014), high osmo-
larity glycerol (HOG) pathway is the main pathway that is responsible for cellular
stress. They reported that Wallemia ichthyophaga and Hortaea werneckii maintain
low intracellular Na+ concentrations by the production of compatible organic
solutes along with glycerol.
To adopt stress condition, fungi also brought changes in membrane properties
that are one of the important mechanisms to survive in harsh environment. One of
the mechanisms used by fungi to survive in the saline environment is the mainte-
nance of membrane fluidity. It has been observed that plasma membrane of salt-
tolerant H. werneckii remained more fluid under varying levels of salinity (Turk
et al. 2004, 2007). They observed that under salinity stress, the total sterol content
of plasma membrane of H. werneckii remained unchanged and their membrane
fluidity was due to modification in the structure of component phospholipids.
Fungi also accumulate polyols and free amino acids as well as their derivatives to
tolerate stress condition.
The above discussion shows that halotolerant microbes use a number of
mechanisms to tolerate saline conditions. One of the common mechanisms used
by these bacteria is the accumulation of compatible solutes. Some species also
accumulate K+ and Ca+2 to maintain ion balance. The presence of some specific
enzymes and metabolites that protect the microbes from harmful effects of salinity
has also been observed.
10.3 Mechanisms of Plant Growth Promotion and

Effectiveness in Stress Agriculture
Environment of rhizosphere differs from bulk soil with respect to its physicochem-
ical properties. In this environment, a number of interactions take place between
plant and microbes. These interactions may be antagonistic and synergistic one
that depends upon the kind of strains involved, and the plant species interact with
this strain. The interactions may take place between plant and bacteria or plant and
fungus and/or between fungus and bacteria. In synergistic interactions, which are a
kind of mutulistic association, both partners help each other by providing benefits,
and ultimately, improvement in plant growth-promoting traits of microbes
occurred (Finlay 2007; Beattie 2007; Franche et al. 2009; Nadeem et al. 2014;
Shin et al. 2016).
Soil microbes and plants interact with each other for growth and survival.
Plants have developed beneficial association with different microorganisms in
rhizosphere which ultimately reduces the stress outcomes (Badri et al. 2009).
Halotolerant microbes including plant growth-promoting rhizobacteria (PGPR)
and fungi can play significant role by protecting the plant from salinity-induced
negative impact (Lugtenberg and Kamilova 2009). As far as the mechanism of
plant growth promotion by these microbes is concerned, generally, the
halotolerant microbes reduce the harmful effect of salinity on plant growth by
improving the production of osmolytes, exopolysaccharides, siderophores, and
phytohormones, enhancing antioxidant enzymes activities, solubilizing the
essential nutrients, improving nutrient acquisition, water use efficiency, and root
hydraulic conductivity. Some selected recent examples of the effectiveness of
halotolerant bacteria and mycorrhizae on plant growth in saline environment have
been presented in Tables 10.1 and 10.2, respectively.
The bacteria in the rhizosphere can improve plant growth by colonizing the
plant roots and these bacteria can promote the plant growth by number of their
direct and indirect mechanism (Muthukumarasamy et al. 2007). Solubilization of
phosphate and potassium by the bacteria, presence of ACC-deaminase, and
production of indole-3-acetic acid (IAA), exopolysaccharides, hydrogen cyanide
(HCN), proline, and siderophores facilitate the plant growth promotion under
saline conditions (Mohamed and Gomaa 2012; Nunkaew et al. 2014; Palaniyandi
et al. 2014; Munoz et al. 2014; Kang et al. 2014a, b). Among a number of
bacterial strains, Bacillus and Pseudomonas are widely used for enhancing plant
stress tolerance against salinity. Pseudomonas putida UW4 showed significant
increase in shoot fresh weight of canola compared to uninoculated plants at 150
mM NaCl (Cheng et al. 2007). Salinity-tolerant bacterial strains could be a good
option to reduce salinity-induced impact on growth of plant. Due to the presence
of salinity-tolerant gene, these bacteria have the ability to develop successful
interaction with plant. Reduction in deleterious effect of salinity and improved
plant growth of wheat have been observed when it was inoculated with gfp-tagged
Azospirllum lipoferum (Bacilio et al. 2004).
Table 10.1 Inoculation of PGPR for inducing salinity tolerance in plants

Crop Bacterial strain Response/mechanisms Reference
Oryza sativa Curtobacterium albidum Improved proline contens, Vimal et al.
SRV4 strain membrane stabilization (2018)
index, and efficacy of
photosynthetic pigments
Enhanced antioxidative
enzymatic activity and K+
uptake in paddy plant
correlated
Reduce stress-induced
ethylene by ACC
deaminase activity and Na+
availability by EPS
production
Enterobacter sp. P23 Decrease in antioxidant Sarkar et al.
enzymes and stress-induced (2018)
ethylene
Phosphate solubilization
IAA production and
siderophore production
Bacillus Improved the membrane Tiwari et al.
amyloliquefaciens NBRI- integrity (2017)
SN13 (SN13) Improved accumulation of
osmoprotectants
Improved the expression of
marker genes
Lysinibacillus sp. (BPC2) Increased plant dry weight, Kumar et al.
and Pseudomonas plant fresh weight, and (2017)
aeruginosa (PRR1 and secondary root number
PHL3) Increased chlorophyll
contents
IAA production and
Brassica napus L. Enterobacter cloacae Increased chlorophyll Li et al.
HSNJ4 contents, amount of lateral (2017)
roots, shoot length, and root
length
Decreased MDA content
Increased activities of
antioxidant enzyme and
proline content
More endogenous IAA
content
Reduced ethylene emission
by ACC deaminase activity
Citrullus lanatus, Bacillus sp. LBEndo1 and More growth both under Palacio-
Arabidopsis Pseudomonas lini normal conditions and in Rodríguez
KBEcto4 salinity stress et al. (2017)
(continued)

thaliana, and Expression of inductive
Cucumis sativus gene construct in response
to auxins and more auxin
contents in roots
IAA production and
Capsicum Pseudomonas Reduced ethylene emission Chatterjee
annuum frederiksbergensis OS261 by ACC deaminase activity et al. (2017)
More activities of
antioxidant enzymes
Reduction in concentration
of H+ ion
Arabidopsis Burkholderia More proline contents Pinedo et al.
thaliana phytofirmans PsJN Upregulated the gene (2015)
expression that are
associated with ROS
scavenging (Ascorbate
peroxidase 2)
Upregulated the gene
expression that are
responsible for abscisic acid
signaling (Relative to
Dessication, RD29A and
RD29B)
Upregulated the gene
expression that is
responsible for
detoxification (glyoxalase I
7)
Downregulated the gene
expression that are
responsible for jasmonic
acid biosynthesis
(lipoxygenase 2)
Altered the expression
pattern of ion homeostasis-
related genes (high-affinity
K+ transporter
1, Arabidopsis K+
transporter 1, Arabidopsis
salt overly sensitive 1, and
sodium hydrogen
exchanger 2)
Arachis hypogaea Genera of Pseudomonas, Increased total nitrogen and Sharma et al.
Klebsiella, more growth (2016)
Ochrobactrum, and Balancing of ion
Agrobacterium homeostasis
(continued)

Reduced ROS
accumulation
IAA production and
phosphate solubilization
ACC deaminase activity
Triticum Stenotrophomonas Increased chlorophyll Singh and
aestivum L maltophilia SBP-9 content Jha (2017a,
Decreased MDA as well as b)
proline contents
More activities of
antioxidant enzymes like
CAT, SOD, and POD
Decreased concentration of
Na+ contents roots and
shoots
Increased the K+ uptake
Rhizobium tropici strain Augmented the activities of Fukami et al.
CIAT 899 and antioxidant enzymes (2018)
Azospirillum brasilense responsible for
strains Ab-V5 and Ab-V6 detoxification of ROS like
CAT, SOD, and APX
Decreased MDA and
poroline contents
Modulated the gene
expression (in general
upregulated) that are
responsible for activities of
SOD2, APX1, SOD4, and
CAT1 in leaves while APX2
in roots
Downregulated the gene
expression that is related to
pathogenesis like prp2,
PR1, and prp4
Downregulated the
expression of gene hsp70 in
leaves and roots that is
related to heat shock protein
Klebsiella sp. SBP-8 Increased contents of total Singh et al.
proteins, soluble sugars as (2015) and
well as proline Singh and
Decreased the Jha (2017a,
concentration of salinity- b)
induced MDA content
More activities of
POX, CAT, and SOD
(continued)

Na+ exclusion and
increased uptake of K+ in
the host plant
Increased plant biomass and
chlorophyll content
Beta vulgaris L. Variovorax paradoxus, More plant biomass and Zhou et al.
Planococcus rifietoensis, seed germination (2017)
and Micrococcus More photosynthesis
yunnanensis Decreased production of
stress-induced ethylene
Decreased host ACC by
ACC-deaminase activity
Solanum Bacillus pumilus AM11 Higher biomass Ali et al.
lycopersicum and Exiguobacterium Increased photosynthetic (2017)
sp. AM25 rate
Increased pigment
accumulation
Decreased lipid
peroxidation,
Increased glutathione,
catalase, and peroxidase
activities
Pisum sativum L. Planomicrobium sp. Decreased levels of ROS Shahid et al.
MSSA-10 Enhanced antioxidative (2018)
enzyme activities
Increase in chlorophyll and
protein contents
Auxin production
ACC deaminase activity
In order to minimize the adverse effect of salinity, plants accumulate ions in its
vacuole, and ion balance is maintained by accumulation of counterions. For exam-
ple, to neutralize the impact of Na + ions accumulated in the vacuole, plant
sequestered organic solutes and K+ into the cytoplasm (Hasegawa et al. 2000).
Inoculation of plant with bacteria under salinity stress causes reduction in Na +/K+
ratios. The inoculated bacteria enhance the uptake of K+ and decrease Na+ concen-
tration in the tissue. The low value of Na+/K+ ratios shows the capability of
bacteria to enhance uptake of K+ (Govindarajan et al. 2006).
Enhancing the accumulation of organic solutes in plant under salinity stress is
also a well-adopted mechanism used by bacteria to improve plant growth. Under
stress, bacteria induce the plants to produce compatible solutes. These low
molecular weight compounds protect the cell from hyperosmotic stress.
Accumulation of
Table 10.2 Inoculation of mycorrhizal fungi for inducing salinity tolerance in plants
Crop Fungal strain Response/mechanism Reference
Sesbania Funneliformis mosseae (syn. Improvement in nodules number Abd-
sesban Glomus mosseae); and weight Allah
Rhizophagus intraradices Enhanced nitrogenase activity et al.
(syn. Glomus intraradices) Reduced oxidative damage by (2015)
and Claroideoglomus scavenging ROS
etunicatum (syn. Glomus Increase level of phytohormones
etunicatum) (IAA, IBA and GA3) and non
enzymatic antioxidants
Oryza sativa Claroideoglomus etunicatum Extrusion of Na+ from the Porcel
(isolate EEZ 163) cytoplasm et al.
Sequestration of Na+ into (2016)
vacuole and its unloading from
xylem
Decreased root-to-shoot Na+
distribution
Claroideoglomus etunicatum Enhanced photosynthetic, Porcel
(isolate EEZ 163) stomatal conductance, and et al.
transpiration (2015)
Enhancing the quantum yield of
PSII photochemistry and
reducing the quantum yield of
non-photochemical quenching
Triticum Glomus mosseae, Regulate the uptake of sodium Mardukhi
aestivum L. G. intraradices, and (Na+) and chloride (Cl—) et al.
G. etunicatum Increased the uptake of essential (2015)
macro- and micronutrients
Nicotiana Rhizophagus irregularis Increased respiration via Del-Saz
tabacum cytochrome oxidase pathway et al.
(COP) (2017)
Higher synthesis of ATP
Higher biomass production
Improved P accumulation and
favoring both ATP production
and shoot growth
Cicer Funneliformis mosseae Improved growth, yield, and Garg and
arietinum L. nutrient uptake Bhandari
Protection of chlorophyll (2016)
pigment from damage
Increased the activity of
RUBISCO (ribulose
1,5-bisphosphate carboxylase
oxygenase)
Osmium Glomus deserticola Improved balance between K/Na Elhindi
basilicum and between Ca/Na et al.
Improvement in chlorophyll (2017)
content, photosynthetic
(continued)

Crop Fungal strain Response/mechanism Reference
efficiency gas exchange, and
water use efficiency
Glomus clarum Nicol. & Produced more biomass Elhindi
Schenck Increased the accumulation of et al.
nutrients, reducing sugars, total (2016)
soluble carbohydrates,
photosynthetic pigments,
proline, and protein
Reduced the Na+ accumulation
Cajanus Funneliformis mossseae and Improved nutrient uptake Garg and
cajan (L.) Rhizophagus irregularis Significant improvement in Pandey
Millsp. biomass and yield (2015)
Improved membrane stability
Funneliformis mosseae Strengthen the antioxidant Garg and
system Chandel
Modulated the nonenzymatic (2015)
components (GSH-GSSG
cycling, their ratio, and total
glutathione)
Sesbania Funneliformis mosseae (BGC Decreased H2O2 concentration Kong
cannabina NM03D) The induction of strigolactone et al.
accumulation (2017)
Regulated strigolactone-induced
salt stress tolerance
Puccinellia Funneliformis mosseae and Increased plant biomass Liu et al.
tenuiflora Claroideoglomus etunicatum Increased shoot P and K (2018)
concentrations,
Reduced shoot Na+
concentrations
Arundo Funneliformis mosseae and Increased the proline Pollastri
donax, Rhizophagus irregularis accumulation and et al.
Higher isoprene emission and (2017)
higher H2O2
Citrus G. mosseae and Decreased intercellular CO2 Navarro
macrophylla G. intraradices levels and oxidative stress et al.
Increased total chlorophyll (2015)
Increased the water percentage in
leaves
Leymus Glomus mosseae (BGC Increased plant biomass, Lin et al.
chinensis HEB02) Higher photosynthetic (2017)
parameters and
Increased contents of
photosynthetic pigments
glycine, proline, betaine, glutamate, and trehalose has been observed in

Azospirillum to minimize the salinity effect (Tripathi et al. 2002). Inoculation of
PGPR significantly enhanced the concentration of soluble sugar and proline in
the leaves and root of salinity-stressed plant (Azarmi et al. 2016). The
accumulations of these compatible solutes enable the plant to maintain growth.
Similarly, the role of soluble protein for maintaining osmotic adjustment, internal
water potential, and cell turgidity has also been reported (Tester and Davenport
2003). Plant growth under salinity is also improved by inoculating salinity-tolerant
bacterial strains that increase the water potential and decrease electrolyte leakage
as well as reduce the sodium concentration (Kang et al. 2014a, b).
Syntheses of the exopolysaccharides (EPS) by the rhizospheric bacteria
promote soil aggregation. High population density of exopolysaccharide-
producing bacteria in the rhizosphere could be helpful for minimizing the salinity-
induced impact on plant. Stabilization of soil structure and aggregation formation
were also observed through the exopolysaccharides produced by the bacteria
(Gouzou et al. 1993). The inoculation of exopolysaccharides producing
Pseudomonas mendocina improves the plant growth in saline environment by
reducing Na+ availability for plant uptake (Kohler et al. 2006).
Exopolysaccharides produced by the bacteria play a significant role to reduce the
Na+ availability for uptake of plant. Decrease in Na + uptake was also observed by
Ashraf et al. (2004) due to the inoculation of bacterial strain having the ability to
produce exopolysaccharides.
Bacteria produce different compounds including phytohormones such as
auxins, gibberellins, cytokinin, as well as siderophores and antimicrobial
compound which play a role in mitigating the negative impact of biotic and abiotic
stress (de-Salamon et al. 2001; Mitter et al. 2013; Cassan et al. 2014). Better
seedling growth and relatively higher auxin contents were observed when wheat
seeds were inoculated with salt-tolerant bacteria and then grown in saline
conditions (Afrasayab et al. 2010). Mazhar et al. (2013) also reported the
beneficial effect of auxins producing cyanobacteria. The inoculation enhanced the
seedling biomass by causing positive impact on root and shoot length.
Under salinity stress, high ethylene produced negatively affects the root length
of plant, and inhibition in root elongation is observed (Abeles et al. 1992). Among
different growth promoting traits of rhizospheric bacteria, the presence of ACC-
deaminase enzyme could be one of the best traits that play a key role in
minimizing the stressed induce ethylene on root growth and ultimately plant main-
tain its proper growth in salty environment (Nadeem et al. 2010a, b; Glick 2010).
The bacteria containing this enzyme, i.e., ACC-deaminase, cause reduction in
internal plant ethylene concentration by hydrolyzing its immediate precursor, i.e.,
1-aminocyclopropane-1-carboxylate (ACC), and therefore promote plant growth
by stimulating root elongation (Glick et al. 1995, 1999). An improvement in
cucumber growth has been reported in the presence of 75 mM salt concentration
due to inoculation of bacteria containing ACC-deaminase (Gamalero et al. 2010).
Simi- larly, in addition to its positive effect on root length and seedling biomass of
tomato, enhancement in germination percentage has also been observed by
inoculation with salt-tolerant bacteria containing ACC-deaminase
(Chookietwattana and Maneewan,
2012). Salt-tolerant Planococcus rifietoensis promoted the wheat growth and yield
under saline conditions (Rajput et al. 2013). The strain was able to grow up to 65
g/L NaCl concentration and showed its potential to hydrolyze ACC by using it as
sole source of nitrogen as well as solubilizing phosphorus from insoluble source
(tricalcium phosphate). On overall basis, 37% increase in plant growth was
observed under salt stress. However, in the presence of inorganic tricalcium
phosphate, the growth enhancement was 63%, and more than 60% increase in
growth was noted when ACC was added in the medium. This showed that growth-
promoting ability of strain also depends upon other factors. A number of other
studies conducted by various workers in the saline environment also mentioned
the potential of ACC-deaminase bacteria in lowering the level of stress-induced
ethylene (Mayak et al. 2004; Glick et al. 2007; Nadeem et al. 2010a, b, Shin et al.
2016).
Salinity causes oxidative damage to plants by producing reactive oxygen
species (Zhu et al. 2007). Inoculation with halotolerant bacteria enables the plant
to mitigate the impact of reactive oxygen species (ROS) by enhancing antioxidant
enzyme activities. It has been noted that bacterial inoculation enhanced the salinity
tolerance of okra by scavenging the reactive oxygen species and improving water
use efficiency (Habib et al. 2016). A much higher concentration of antioxidant
enzymes including peroxidase, catalase, and nitrate reductase has been observed
under salinity stress in plant inoculated with PGPR (Sen and Chandrasekhar
2015). Prior to this, Jha and Subramanian (2013) also found an improvement in
growth parameter through inoculation with PGPR under salinity. The inoculated
bacteria regularized the ion concentration and enhanced the activities of
antioxidant enzymes.
Similar to bacteria, arbuscular mycorrhizal (AM) association with plants is also
one of the most widespread beneficial associations that protect the plants from
biotic and abiotic stresses by their direct and indirect mechanisms. Inoculation of
Citrus reticulata (red tangerine) by Paraglomus occultum and Glomus mosseae
enhanced the salinity tolerance by improving root morphology, photosynthetic
activity, and maintenance of ion balance (Wu et al. 2010). Similarly, increase in
growth, fresh and dry weight of root, as well as nutrient and water absorption were
also reported by other researcher (Ghoulam et al. 2002; Cho et al. 2006; Al-Karaki
2006).
Mechanisms used by mycorrhizal fungus to increase resistance of host plants
against salinity were intensively investigated (Liu et al. 2015a, b; Wu et al. 2014;
Meng et al. 2015; De Almeida et al. 2016). Mycorrhizal hyphae colonize the plant
root and establish symbiotic relationship. Fungus penetrates into the cortex and
forms specialized structures, i.e., arbuscules, and after colonization of the root of
host plant, the mycelium of the fungus penetrates into soil in search of water and
nutrients (Breuninger and Requena 2004; He and Nara 2007). Ectomycorrhizal
and endomycorrhizal fungi significantly improve seedling growth and biomass of
the inoculated plant under salt-stressed condition (Diouf et al. 2005). Mycorrhizae
dilute the negative impact imposed by the salinity on plant by enhancing the
antioxidant system to mitigate the harmful effect of reactive oxygen species and
reducing oxidative damage (Rabie and Almadini 2005; Manchanda and Garg
2011; Wu et al. 2014; Ahmad et al. 2015a, b), improving nutrient acquisition
especially phosphorus (Meng et al. 2015; Evelin et al. 2009), inducing
acquired systemic
tolerance (Hashem et al. 2016a), enhancing water uptake (Ruiz-Lozano and Azcon
2000), improving osmolyte production (Ibrahim et al. 2011; Evelin et al. 2013),
reducing the uptake of harmful ions such as Cl— and Na+ (Al-Karaki 2006; Daei et
al. 2009), maintaining ion balance by improving uptake of nutrients and
stimulating selective uptake (Evelin et al. 2012), improving water use efficiency
(Hajiboland et al. 2010), and altering root morphology to increase water and
nutrient absorption
(Aroca et al. 2013; Ahanger et al. 2014).
Mycorrhizal fungi reduced the salinity-imposed negative impact on growth of
Cucumis sativus L (Hashem et al. 2018). They demonstrated that fungus
strengthens the plant antioxidant system and therefore reduces the harmful impact
of ROS by accelerating the activity of antioxidant system. Earlier studies
conducted by various workers also showed that mycorrhizal association is helpful
for maintaining plant growth in the salt-stressed environment by improving the
antioxidant system of plant (Alguacil et al. 2003; He et al. 2007). Sarwat et al.
(2016) demonstrated that salinity tolerance of B. juncea seedlings was due to
improvement in antioxidant system, reorganization of the physiological and
biochemical parameters, as well as production of secondary metabolites and
phytohormones. Yang et al. (2014) also documented an enhancement in the
activity of ascorbate peroxidase and catalase enzymes in mycorrhizal inoculated
plants compared to non-mycorrhizal in saline conditions. Abd-Allah et al. (2015)
while studying the impact of myccorhizae on Sesbania Sesban under saline
conditions observed that an improvement in the growth and yield parameters of
Sesbania was due to activation of antioxidant system and nonenzymatic
antioxidant as well as production of phytohormones.
Superoxide dismutase (SOD) stabilizes the membrane of plant cells by
regulating the ROS. Plants having symbiotic relationship with R. irregularis have
greater SOD activity that reduced the level of lipid peroxidation and provide
protection to the plant membrane against damage. Lower ROS in plants having
mycorrhizal connection is due to rapid ROS-scavenging enzymes, i.e., catalase
and guaiacol peroxidase (Pandey and Garg 2017). Higher isoprene emission
linked with more accumulation of ROS and more H2O2, especially in plants
colonized by R. irregularis (Pollastri et al. 2017). In tomato, due to mycorrhizal
association, antioxidants, e.g., peroxidase, catalase, etc., are produced which cause
degradation of ROS under salt stress condition (He et al. 2007).
Salt stress on plants affects various physiological processes of plant such as gas
exchange, efficiency of photosynthetic system, water and nutrient absorption, and
permeability of membrane (Aroca et al. 2006; Porcel et al. 2006). Mycorrhizae
improve the plant physiological processes by enhancing water absorption owing to
its positive role in enhancing root hydraulic conductivity (Ruiz-Lozano and Azcon
2000; Ruiz-Lozano 2003). Similarly, root colonization of G. intraradices dilutes
the impact of salinity and protected the leaf from dehydration. Lower water satura-
tion deficit and higher turgor potential in mycorrhizal plants also improved the
water status of the plant (Sheng et al. 2008; Al-Garni 2006). Relatively high water
content has been observed in mycorrhizae-inoculated plants that was due to
improved root hydraulic conductivity at low water potential (Sheng et al. 2008;
Jahromi et al. 2008; Kapoor et al. 2008). These changes in physiological processes
improve the growth of plants by protecting them from negative impact of toxic
ions as it was observed in case of Solanum lycopersicum where mycorrhizae
mitigated the negative effect of salinity on plants (Balliu et al. 2015; Hashem et al.
2016a, b, c). Better root colonization of Cucurbita pepo plants was observed by
inoculation with Glomus intraradices under salinity stress which improved
growth, yield, and quality of fruit compared to uninoculated by enhancing water
and nutrient status (Colla et al. 2008). Root colonization of Lotus glaber by
mycorrhizal fungi also facilitated the growth of said plant (Sannazzaro et al.
2007). High value of electrical conductivity was observed in the root of
mycorrhizal plants (Garg and Manchanda 2008). Maize inoculated with
mycorrhizal showed higher electrolyte permeability of root plasma membrane that
was due to high production of antioxidant enzyme and uptake of phosphorus
(Feng et al. 2002).
Rate of photosynthesis is reduced under salinity stress. Mycorrhizal plants have
more ability to fix CO2 that’s why their growth improved (Querejeta et al. 2007).
Inoculation of mycorrhizae restored the chlorophyll activity in the presence of
salinity that was due to the activity of specific enzymes (Hajbagheri and Enteshari
2011). High chlorophyll content has been observed under saline condition in the
leaves of mycorrhizal plants (Sannazzaro et al. 2006; Sheng et al. 2008).
Mycorrhi- zal symbiosis increased the chlorophyll contents and photosynthetic
capacity of corn crop under salt stress conditions (Sheng et al. 2008). Efficiency of
photosynthetic system enhanced due to regularizing the energy bifurcation and
improving efficiency of photochemical and non-photochemical PSII. Borde et al.
(2010) also observed the enhancement of photosynthesis rate in garlic plants under
salt stress. In mycorrhizal plant, absorption of Mg was increased that improved the
synthesis of chlorophyll. For better functioning of photosynthetic machinery, the
mycorrhizae inhibited the Na+ transport and therefore increased photosynthesis
rate (García-Garrido and Ocampo 2002). Recently, Sharma et al. (2017) observed
that inoculating the plant with mycorrhizae enhanced the growth of plant by
causing positive impact on nutrient uptake, photosynthetic pigments, phosphatase,
and peroxidase activity. They found that mycorrhizae also decreased the
membrane damage. Elhindi et al. (2017) also demonstrated that mycorrhizae
enhanced the plant growth under saline condition that was linked with gas
exchange, photosynthetic efficiency, and water use efficiency.
Mycorrhizae can also minimize the negative impact of stress on plant by
altering the hormone level of the plant. Abscisic acid that is an important growth
hormone plays a significant role in salinity tolerance. Mycorrhizae have the ability
to alter the ABA level of inoculated plant (Bothe et al. 1994; Estrada-Luna and
Davies 2003) that could be helpful for maintaining growth of plant in saline
conditions. Similarly, the higher cytokinin level was also observed in root and
shoots in plants inoculated with mycorrhizae (Allen et al. 1980). Allen et al.
(1980) also reported the improvement in growth due to improvement in the
content of cytokinin.
The accumulation of carbohydrate under stress is another mechanism to
maintain proper plant growth. The inoculation of Phragmites australis with
mycorrhizae Glomus fasciculatum caused a significant increase in carbohydrate
(Al-Garni 2006). The work of Porcel and Ruiz-Lozano (2004) also reported
similar results
when soybean was inoculated with Glomus intraradices. Evelin et al. (2009)
observed high soluble sugar content in mycorrhizal plant when compared with
non-mycorrhizal one.
Salinity reduces the absorption of mineral nutrients particularly phosphorus due
to its precipitation with Ca+2 and Mg+2. Due to very small diameter of the
mycelium, it can penetrate into soil and extend outside the rhizosphere and
therefore increase the root surface area for nutrient absorption. Such fine roots and
improved root surface area are very helpful for the plant to uptake nutrients and
water from the stress environment. According to an estimate, up to 80%
phosphorus
(P) requirements of plant are fulfilled by the activity of external hyphae of
mycorrhizae (Matamoros et al. 1999). Therefore mycorrhizal plant has
competitive advantage over non-myccorhizal plant and has better ability to survive
in the stress conditions. Plenchette and Duponnois (2005) and Sharifi et al. (2007)
also reported the improvement in plant growth by improving nutrient acquisition
particularly the availability of phosphorus.
Mycorrhizal fungi are also important in maintaining ion homeostasis during salt
stress condition (Estrada et al. 2013). Mycorrhizal fungus enhanced halotolerance
of plants through improving plant nutrition, more K +/Na+ ratio in plant tissue,
improved photosynthesis and water use efficiency (WUE), production of
osmolytes, compartmentalization for ion storage, and protecting enzyme activity
(Rabie and Almadini 2005; Al-Karaki 2006; Porcel et al. 2012). High ratio of
K/Na is an indication of salinity tolerance, and inoculation with mycorrhizae is
also helpful to maintain a high K/Na ratio in saline conditions (Giri et al. 2007;
Zhang et al. 2011). Mycorrhizal fungus Glomus deserticola improved water use
efficiency and balance between K/Na and between Ca/Na in sweet basil plants
during saline conditions (Elhindi et al. 2017). Yang et al. (2014) also observed
relatively high K/Na ratio in
mycorrhizal plants as compared to non-mycorrhizal plants. Mycorrhizal fungi
reduce the salinity stress by discouraging the uptakes of Na+ and Cl—, their
transport toward plasma membrane, tonoplast, and their movement toward shoots
(Al-Karaki 2006; Lee et al. 2015).
Mycorrhizal fungus has the ability to minimize the salinity-induced impact and
enhance crop productivity (Evelin et al. 2009; Garg and Pandey 2015).
Mycorrhizal fungi form association with legume plant Sesbania cannabina which
improved its resistance to soil salinity (Ren et al. 2016). Fine-tuned coordination is
needed at molecular level for successful establishment of plant-mycorrhizae
association (Andreo-Jimenez et al. 2015). Mycorrhizal fungus increases
strigolactone (SL) levels of plant and is responsible for the increased salt
resistance and even restored the biomass and photophysiological damage (Kong et
al. 2017). Strigolactone role as signal molecule in rhizosphere has been already
proven and detected in plant root extracts (Xie et al. 2010). In lettuce plants,
increase in strigolactones levels was also noticed during salt stress in mycorrhizal-
inoculated Rhizophagus irregularis (Aroca et al. 2013). It has been observed that
plants not only produce a single strigolactone but also blend of various SLs
depending on a plant species (Xie et al. 2010; Ruyter-Spira et al. 2013). Different
studies have proved that less H2O2 concentration is also a mechanism used by
fungi to support crop growth
against salt stress (Hajiboland et al. 2010; Garg and Bhandari 2012). One
important thing to remember is that increased concentration of H2O2 acts as an
oxidative agent, whereas a low concentration may act as a signaling molecule (Xia
et al. 2009; Torres and Dangl 2005). In Sesbania cannabina seedlings,
accumulation of H2O2 was noticed against salt stress after mycorrhizal fungal
colonization. Strigolactone induces halotolerance by a complex set of signal
transcription pathways. In this H2O2 is used as a common signal molecule and is
produced as a result of NADPH oxidase activation during salt stress conditions in
mycorrhizal plants (Kong et al. 2017). Plant roots are the part of plant which
mostly experience the salinity stress and so
produce more reactive oxygen species (ROS) as compared to leaves. ROS (O2 —,
H2O2) have high potential to cause peroxidation of lipids membrane present in the
intercellular organelles and cell membrane (Pedranzani et al. 2016).
Mycorrhizal fungal species Funneliformis mosseae and Rhizophagus
irregularis improve plant’s performance and prevent damage under salt stress by
increasing proline production which is one of the well-known scavengers of free
radicals and acts as buffer during stresses (Porcel et al. 2012; Pollastri et al. 2017)
and is known as the best compatible solutes those balancing the salt accumulated
in plants and being currently used by biotechnologists for salt tolerance in plants
(Szabados and Savoure 2010; Deinlein et al. 2014). Other scientists have already
mentioned high proline content in mycorrhizal plants (Jindal et al. 1993; Sharifi et
al. 2007). Sharifi et al. (2007) demonstrated that a high concentration of proline in
the root of mycorrhizal soybean plant compared to shoot under saline conditions
might be due to the reason that roots play a key role in water absorption and
maintain osmotic balance between internal and external environment. Glycine
betaine is another osmoprotectant produced by several plants during stress
conditions including salinity stress. Betaines play important part in stabilizing
the enzymes, protein complexes, and membrane integrity against salt stress.
Considerably more betaine contents were recorded in mycorrhizal plants (Al-
Garni 2006).
Piriformospora indica produced cytokinin and was involved in halotolerance of
host plant through its cross talk with abscisic acid (Crafts and Miller 1974;
Nishiyama et al. 2011). Abscisic acid is a phytohormone important for plant
growth, development, and even abiotic stresses, i.e., salinity. ABA accumulation
has been reported to be altered in plants having mycorrhizal association (Estrada-
Luna and Davies 2003). Fungi also produce ACC-deaminase in order to degrade
ethylene precursor ACC in order to rescue normal plant growth and regulate
expression of hkt1leading to Na+ homeostasis during salt stress (Contreras-
Cornejo et al. 2009; Viterbo et al. 2010).
Jatropha curcas inoculated with mycorrhizae showed normal water content in
leaves and improved water conductance in root of stress plant (Kumar et al. 2015).
In a greenhouse experiment, two date palm cultivars (Nakhla hamra and Tijib)
inoculated with five different species of mycorrhizae (G. intraradices,
G. aggregatum, G. mosseae, G. verriculosum, G. fasciculatum) and subjected to
salinity (Diatta et al. 2014). The cultivar showed variable response to salinity and
mycorrhizae species. It has been observed that Nakhla hamra inoculated with
G. intraradices showed better growth under salinity stress, while Tijib grew better
when inoculated with G. fasciculatum. Salt stress ability of cultivar was due to
accumulation of compatible solute, i.e., proline. The concentration of proline

depends upon the species of mycorrhizae and the intensity of the salinity.
Recently, Manga et al. (2017) also found variable response regarding the
performance of mycorrhizae under saline environment. While testing the efficacy
of eight mycorrhizal fungi to enhance salinity tolerance of Acacia seyal, they
observed that efficiency of mycorrhizae was variable in improving mineral
nutrition and it depends upon the type of mycorrhizae associated with seedlings as
well as salinity level. They suggested that interaction between plant and
mycorrhizae can be modulated by the type and diversity of mycorrhizae as well as
intensity of abiotic stress. It has observed that inoculation of mycorrhizae not only
promoted the plant yield but quality of fruit also improved (Kaya et al. 2009).
It has also been observed that all fungi do not have the similar ability to reduce
the salinity-induced impact on plant. In some cases mycorrhizae don’t save the
plant from harmful effect of salinity due to the reason that mycorrhizae were not
able to maintain its proper growth and its activity affected under salt stress
conditions (Juniper and Abbott 2006; Sheng et al. 2008). There is variability
among fungal species to grow in stress environment. Nazareth et al. (2012), while
studying the metal resistance of halotolerant fungi isolated from mangroves and
salterns of Goa, India, reported that species belonging to Penicillium showed
highest levels of halotolerance as well as resistance to heavy metals compared to
Aspergillus. Species belonging to genera Paecilomyces showed a lower
halotolerance. They demonstrated that mechanism of tolerance in fungi was
phylogenetically related.
10.4 Synergistic Application of Halotolerant Microbes
In spite of the use of PGPR since long, their survival in the rhizosphere by
competing with native microflora as well as their abilities for effective
colonization of the rhizosphere remain unexplored and need to be further
investigated for making this approach successful (Bashan 1998). Moreover, higher
concentration of salts in soil could further cause problems for microbes to
maintain their activity and survival (Bremer and Kramer 2000). Performance of
single microbial strains/agents often remains inconsistent in field evaluation by
reason of less population counts of introduced single microbial strains and their
competition with aboriginal microbial population (Felici et al. 2008). Additionally,
different environmental factors (including both biotic and abiotic) and rapid
reduction of introduced microbial population counts also lead to inoculum failure.
Soil microbiostasis causes rapid decrease of introduced microbial strains
(Johannes et al. 1997). Effectiveness and stability of single microbial strain used
for inoculation could also be one of the major problems of inoculums failure.
Hence, more efforts are needed to increase the survivability of introduced
microbes in the rhizosphere especially under unfavorable environmental
conditions.
The use of beneficial microbes in their two or more combinations increases
their reliability because of better established microbial community in the
rhizosphere,
multiple synergistic mechanisms, and improved survivability in various kinds of

environmental conditions (Larkin and Fravel 1998). Multi-strain inoculation of
microbes has pronounced effect for improving plant growth as compared to
individual inoculations of microbial strains. This additive stimulatory effect of
multi-strain microbial inoculation is due to synergy between two or more
beneficial bacteria and/or beneficial fungi/mycorrhizae which possess various
plant growth-promoting mechanisms/activities like production of phytohormones,
enhancing availability of nutrients (Raja et al. 2006), nitrogenase activity (Alam et
al. 2001), and colonization of endosphere by endophytic bacteria (Govindarajan et
al. 2007). Mixed inoculation of microbes not only improved growth of plant in
normal condition, but they also induced systemic tolerance under stressed
conditions (Ruiz-Sanchez et al. 2011). The impact of co-inoculation of bacteria
and mycorrhizal fungus on growth of plant in saline conditions has been
mentioned in Table 10.3.
Multiple ranges of metabolic activities of microbial consortium are mainly
responsible for synergistic effects of microbes to improve plant growth as
compared to their soil inoculation (Adesemoye and Kloepper 2009). Combined
additive effect of multi-strain microbes of consortium on plant growth could be
enhanced through biosynthesis of phytohormones, N2 fixation, and increased
release of sugars and amino acids from roots (Raja et al. 2006; Ruiz-Sanchez et al.
2011). More grain weight and grains per spike in wheat were observed in response
to combined inoculation of arbuscular mycorrhizae and Azotobacter as compared
to their sole inoculations as well as un-inoculated control. This improvement in
grain yield of wheat could be linked to better efficiency of microbial inoculants to
explore additional soil volume (Bahrani et al. 2010). Combined application of
Mesohizobium and Bacillus enhanced the number of tillers, spike length, and grain
yield of wheat due to better uptake of phosphorus. Akhtar et al. (2013)
documented that co-inoculation of Rhizobia and Bacillus enhanced the phosphorus
availability. Further, it has been observed that co-aggregation of Azospirillum
brasilense and Methylobacterium sp. results in improved tomato growth as
compared to their individual inoculation of these strains (Joe et al. 2014). Induced
salinity tolerance in lettuce has been reported by co-inoculation of Serratia sp. and
Rhizobium sp. with improved activities of ascorbate peroxidase and glutathione
reductase. Besides mineral contents and photosynthetic rate were also more by
combined inoculation as compared to use of single strains (Han and Lee 2005).
Afrasayab et al. (2000) also observed that multi-strain inoculation of microbes
caused more improvement in growth of wheat under saline condition which might
be attributed to more auxins, soluble protein contents and K + contents, as well as
decreased concentration of Na+ contents. Bulut (2013) reported that combined use
of different microbial strains results in the improvement of wheat growth almost
equal to that was observed in response of chemical fertilizers. This increase in
growth of wheat due to multi-strain bacterial inoculation was due to more uptake
of nitrogen as compared to individual use of these bacterial strains. Bacterial
consortium of Pseudomonas flourescens, Azospirillum lipoferum, and Bacillus
megaterium enhanced the efficiency of these bacterial strains for effective
Table 10.3 Co-inoculation of PGPR and mycorrhizal fungi for inducing salinity tolerance in
plants
Response/
Crop Fungal strain PGPB strain mechanism Reference
Cajanus Funneliformis Sinorhizobium Higher biomass Garg and
cajan mosseae and fredii strain AR-4 accumulation, Pandey
Rhizophagus nodulation, N2 (2016)
irregularis fixation, and N and P
uptake
Higher AM
colonization
Higher trehalose in
nodules due to
decreased trehalase
and increased
trehalose-6-P
synthase, trehalose-
6-phosphatase
activities
Zea mays L. Glomus etunicatum Methylobacterium Increased dry Lee et al.
oryzae CBMB20 biomass, AMF root (2015)
colonization, and
nutrient
accumulation
Reduced proline
content and Na
uptake
Gigaspora Pseudomonas Improved plant dry Selvakumar
margarita S–23 koreensis S2CB35 weight, nutrient et al. (2018)
and content of shoot and
Claroideoglomus root tissues
lamellosum S–11 Reduced the
accumulation of
proline in shoots and
Na+ in roots
Exhibited high K+/
Na+ ratios in roots
Altered the
expression of
ZmAKT2, ZmSOS1,
and ZmSKOR genes
Acacia Claroideoglomus Bacillus subtilis Enhanced AMF root Hashem
gerrardii etunicatum; (BERA 71) colonization et al.
Benth Rhizophagus Increased in total (2016b)
intraradices; and lipids, phenols, and
Funneliformis fiber content
mosseae Increased content of
osmoprotectants
such as glycine,
betaine, and proline
(continued)

Response/
Reduced lipid
peroxidation
Mentha Glomus Halomonas Highest fresh Bharti et al.
arvensis L. aggregatum, desiderata (STR8) weights (2016a, b)
Glomus mosseae, and Higher oil yield
Glomus Exiguobacterium Better AMF
fasciculatum, and oxidotolerans colonization
Glomus (STR36) Increased nitrogen
intraradices
accretion
Avena Glomus Acinetobacter sp. Decreased the MDA Xun et al.
sativa intraradices and free proline (2015)
contents in plant
Augmented the
activities of the
antioxidant enzyme
(SOD, POD, and
CAT)
Increased the
activities of soil
enzyme (i.e., urease,
sucrase, and
dehydrogenase)
Vicia faba Acaulospora Rhizobium Increased in number Abd-Alla
laevis, Glomus leguminosarum and mass of nodules, et al. (2014)
geosporum, biovar viciae nitrogenase activity,
Glomus mosseae, STDF-Egypt leghaemoglobin
and Scutellospora 19 (R) content of nodule
armeniaca Improved
mycorrhizal
colonization
Increased dry mass
of root and shoot
Phaseolus Glomus mosseae Pseudomonas Higher Younesi and
vulgaris L. (Nicol. & Gerd.) fluorescence concentrations of Moradi
shoots K+ and lower (2014)
concentrations of
shoots Na+
Increased shoots
proline concentration
Increased the
antioxidant enzyme
activities (POX and
CAT)
(continued)

Response/
Ocimum Glomus irradicans Bacillus subtilis Positive effects on Abdel-
basilicum growth, oil %, oil Rahman
yield, and nutrient et al. (2011)
uptake
Glomus Dietzia A positive effect on Bharti et al.
intraradices (Gi) natronolimnaea the indigenous (2016a, b)
STR1 microbial
community structure
Increased the
essential oil content,
oil yield and herb
yield
colonization with improved rice growth by improved biosynthesis of amino acid,

reducing sugars and phytohormones, as well as improved capacity to fix
atmospheric nitrogen (Raja et al. 2006).
Most of the legumes are sensitive to salinity, and symbiotic association of
mycorrhizae with legumes in salinity causes a significant effect on plant and
enhances the ability of inoculated plant to fixation (Garg and Chandel 2011). A
study conducted to assess the effectiveness of co-inoculation of mycorrhizae and
rhizobium to enhance the salinity tolerance of alfalfa showed that combined appli-
cation of two strains increased the yield of alfalfa and a significant increase in
number and weight of nodule was observed (Zhu et al. 2016). The co-inoculated
plants showed more proline content in shoot. The synergistic relationship between
mycorrhizae and bacteria caused an increase in nitrogen and phosphorus content
that enhanced plant nutrition (Giri et al. 2002).
Koc et al. (2016) also studied the role of combined application of bacteria and
mycorrhizae in salinity stress tolerance of strawberry. Increasing salt
concentration reduced all plant growth parameters. The combined application of
mycorrhizae and bacteria ameliorated the salinity-induced negative impact on
strawberry. They observed that co-inoculation protected the plant from salinity
damage by increasing proline and anthocyanin levels. They observed that effect
was more pronounced at higher salinity level. In an earlier study conducted by
Rabie et al. (2005), more effectiveness of mycorrhizae was observed on lettuce at
high salinity level. In many cases, co-inoculation proved useful for improving
crop growth; however, in addition to co-inoculation of two microbial strains,
combined application of mycorrhizae with polyamine also mitigated the negative
effect of salinity. Abdel-Fattah et al. (2013) evaluated the effect of Glomus
mosseae and spermine on growth and physiological aspects of wheat (Triticum
aestivum) by conducting a pot experiment in saline conditions. It has been
observed that dual application of mycorrhizae and spermine caused positive effect
on growth of wheat. The wheat salt tolerance was
associated with better root colonization, enhancement of proline, and protein and
chlorophyll content.
Nutritional imbalance under stress condition affects the growth of plant nega-
tively. High Na+ content in saline conditions inhibits the uptake of essential
nutrients like K+ and Ca+2. Inoculation of plant with mycorrhizae and bacteria
proved useful to enhance the uptake of nutrient and maintain nutrient balance
(Gamalero et al. 2010). Najafi et al. (2012) also reported that co-inoculation of
PGPR-mycorrhizae enhanced the water and nutrient absorption. Due to reduction
of nutrient availability particularly P, the application of mycorrhizae could be
helpful for improving nutrition. Inoculation with mycorrhizae enhanced the
production of antioxidant enzymes, nitrogen fixation, nodule formation, and
ultimately growth and yield of legumes (Garg and Manchanda 2008). Similarly,
mycorrhizae improved the availability and uptake of nitrogen (Govindarajulu et
al. 2005), and according to their view, it might be due to the reasons that microbial
inoculation brought changes in nitrogen metabolism by changing the activity of
enzymes associated with it. In addition to nitrogen and phosphorus, application of
mycorrhizae also enhanced the availability and uptake of essential plant nutrients
including Ca, Mg, K, Cu, Mn, Zn, and Fe (Al-Karaki et al. 2001; Mardukhi et al.
2011).
Co-inoculation of mycorrhizae with bacteria improves nodulation of
subterranean clover and ultimately enhanced the growth (Meyer and Linderman
1986). Mycorrhizae can alleviate salinity-imposed harmful effects on the nitrogen
fixation process and cause significant increased nodules (Giri and Mukerji 2004;
Manchanda 2008). Improved nitrogen fixation under salinity stress was due to
improvement in nitrogenase activity and content of leghemoglobin. Soliman et al.
(2012) while studying the effect of mycorrhizal fungus with Rhizobium observed
that co-inoculation protected the A. saligna plant from salinity-induced negative
impact by decreasing the uptake of Na+ and accumulation of proline.
The interaction between endophytic bacteria and mycorrhizae has been studied
by Hashem et al. (2016b, c) to assess the effectiveness of co-inoculation on the
growth of Acacia gerrardii under salt stress. An increase in root and shoot weight
and number of nodules and leghemoglobin was recorded due to co-inoculation.
Also, inoculated and uninoculated plant showed a significant difference regarding
the activities of nitrogenase and nitrite reductase. Inoculation protected the salt-
stressed
A. gerrardii by enhancing the phosphatase activities and uptake of nitrogen, phos-
phorus, potassium, magnesium, and calcium while reducing the concentration of
sodium and chloride. Similarly, dual inoculation of mycorrhizae and phosphate-
solubilizing fungus (PSF) caused significant impact on phosphate content,
phosphatase activity, and uptake of essential nutrients under NaCl stress
(Xueming et al. 2014). They also observed better root colonization of inoculated
plant than uninoculated one. Phosphate-solubilizing fungus can solubilize the
precipitated P along with K+ and Ca+2 and therefore enhance the availability of
phosphorus in saline conditions (Zhang et al. 2013).
Mycorrhizosphere that is a zone surrounding the plant roots and fungal hyphae
serve as a place of fungal and bacterial interaction (Johansson et al. 2004). The
mutual interactions that occurred among microbial population in this zone not only
affect the plant growth positively but also promoted the survival of each other
(Artursson et al. 2006; Yusran et al., 2009). In this interaction, bacteria by
producing certain compound enhance the cell permeability, stimulate the growth
of hyphae, and facilitate the fungus to penetrate the root penetration (Jeffries et al.
2003). In most of the cases, these interactions are two way and both partners
facilitate each other. Bacterial interactions with fungi facilitate in the development
of mycosymbionts and increase the ability of fungi to colonize the plant roots
effectively (Hildebrandt et al. 2002; Jaderlund et al. 2008). For example, co-
inoculation of Paenibacillus brasilensis with mycorrhizal fungus G. mosseae
enhanced fungal root colonization of clover (Artursson 2005) and mycorrhizae
enhance the phosphorus-solubilizing and nitrogen-fixing ability of the bacteria
(Linderman 1992).
The association between mycorrhizae and plants is strongly affected by
environmental conditions including salinity (Gupta et al. 2000; Cavagnaro et al.
2015), and efficiency of mycorrhizae under such harsh condition can be further
increased by the dual inoculation of mycorrhizae with associative bacteria. Salt-
tolerant Bradyrhizobium caused significant impact on the Vigna radiata L in
saline conditions when it was co-inoculated with Glomus mosseae (Singh et al.
2011). They observed that application of Bradyrhizobium enhanced shoot and root
length, number of nodules, total plant biomass, as well as population and
colonization of arbuscular mycorrhizal fungal (AMF) compared to sole application
of myccorhizae. However, marked increase in growth and yield parameters of
Vigna radiata has been observed by the dual application of these two strains. This
indicates that a synergistic association of arbuscular mycorrhizal fungi and
rhizobia could be very effective to increase the efficiency of plant for nitrogen
fixation that ultimately causes positive effect growth and yield of legumes.
From the above discussion, it can be concluded that co-inoculation of bacteria
and mycorrhizae are useful for promoting the growth of plant under salinity stress.
In such synergistic interactions, both partners help each other for expressing their
growth-promoting traits. Dual inoculation seems to be more effective under stress
conditions because under harsh environment, single strain sometimes do not show
its potential due to unfavorable environment.
10.5 Roles of Halotolerant Microbes in Environmental Science
Environmental contamination is increasing nowaday due to anthropogenic

activities, progressive growth of population, industrialization, and urbanization
(Tabak et al. 2005; Ahemad et al. 2009). The industries which manufacture
pesticide, pharmaceuticals, herbicides, oil, and gas recovery processes produce
wastewaters with salinity fluctuating from time to time. Conventional
microbiological treatment processes don’t function at these salinity variations
because of inadaptability of microbes to varying salt concentration. Due to
involvement of halophilic bacteria in biogeochemical process, these also act as a
biological mediator (Capone 2002). Das et al. (2011) studied the distribution of
halophilic microbes with increasing depth of Sundarban Mangrove forest. These
microbes are involved in the process of
biotransformation biomineralization of soil minerals. According to their

observation, the top soil microbes were more tolerant to salinity fluctuation than
the microbes present in the middle and bottom soil layer. They also observed that
relatively more salinity tolerance ability of anaerobic microbes than top aerobic
microbes present in the bottom segment of soil.
The report of Lowe et al. (1993) indicates that anaerobic bacteria have better
ability to cope with extreme environmental conditions like pH, temperature, and
salinity. Anaerobic microbes having better energy-conserving mechanisms than
aerobic bacteria that make them suitable candidate to adapt harsh environmental
conditions effectively. According to their view, fluctuation in water and salinity
level occurring due to global warming will disturb the activities of aerobic bacteria
more than anaerobic ones.
Microorganisms are ideally suited for cleaning contaminated environment
because certain microbial species containing particular enzymes enable to survive
in contaminated environment by using certain compounds as a food source.
Halotolerant microbes have the ability to tolerate adverse environment, and by
virtue of their particular enzymes, these can be used as bioremediation agents. Qin
et al. (2012) studied bioremediation of petroleum hydrocarbons in saline-alkaline
conditions. They observed that salinity had great impact on bioremediation. At
initial stage, moderate salinity enhanced the biodegradation; however, gradual
increase in salinity decreased the rate of degradation. The addition of mixed
culture of two fungal strains (Trichosporon sp. and Penicillium citrinum) isolated
from saline-alkaline conditions improved the biodegradation efficiency and
dehydrogenase activity. There was a positive correlation between degradation
rate and activity of dehydrogenase enzyme. They suggested that addition of salt-
tolerant inocula is effective for enhancing the bioremediation of hydrocarbon in
saline environment.
Bioremediation potential of salt-resistant Bacillus strains was studied by
Abdughafurovich et al. (2010) under aerobic condition. The study employed the
use of tritium-labeled polychlorinated biphenyls (PCBs) congeners and tracing the
tritium label in cultures with high salt content. The results showed that most of the
Bacillus strains were able to absorb a part of the radioactivity. The results of gas
chromatography showed the transformation of PCBs. They demonstrated that such
strains could be very suitable for bioremediation of contaminated salt-affected
soils. Response of sea water microbial inocula with and without biosurfactants and
micronutrients was evaluated to enhance the bioremediation of hydrocarbon-
contaminated mangrove swamp (Okoro 2010). A significant increase in
bioremediation was observed where microbial inoculum was applied with
biosurfactants and micronutrients.
The work of Arakaki et al. (2013) indicated that salinity inhibits the growth of
seven out of ten fungus strains and three strains Polyporus sp, Dacryopinax
elegans, and Datronia stereoides produced high biomass in saline medium. When
glycerol and mannitol were added in the medium, it enhanced the activity of D.
elegans regarding the biomass production and ligninases. It degraded diuron in the
presence of NaCl as well as polyols. Similarly, among 26 halotolerant isolates, 2
aerobic Bacillus spp. showed resistance and potential for Se (IV) reduction.
Both strains
completely reduced the Se (IV) to selenite within 40 h. Nanosized spherical

particles of selenium were found in and around the bacterial cell which were
further confirmed by confocal micrograph study. They demonstrated that these
microbial strains could be an important source for bioremediation of Se.
Due to rapid increase in textile industry, a number of synthetic dyes are present
in the effluent, and the removal of these dyes from the wastewater is a challenge to
protect the soil from contamination. These dyes not only degrade the soil quality
but also cause negative impact on underground water quality. The use of bacteria
to remove these dyes from the wastewater is one of the promising technologies.
Salinity caused significant impact on bioremediation processes, and the process of
degradation is affected due to negative impact of salinity on microbial population
participating in degradation process. Therefore due to the presence of number of
salts in such water, not all the bacterial strains could be effective for
bioremediation of such dyes. The use of halotolerant bacteria could be very
effective in such conditions due to eco-friendly and an inexpensive strategy
(Parshetti et al. 2006). A number of bacterial strains have been isolated which can
degrade azo dyes. Some of these strains include Exiguobacterium, Klebsiella
pneumoniae, Acinetobacter, and Gracilibacillus (Salah et al. 2007; Tan et al.
2009; Bibi et al. 2012; Agarwal and Singh 2012).
Isolating microorganism from the contaminated environment and then using
these microbes in the same environment for bioremediation purpose is better
strategy to clean the environment. The isolation of bacterial strains from saline
conditions and then their application to remove azo dyes have been evaluated by
Lalnunhlimi and Krishnaswamy (2016). A consortium of bacterium at various
concentrations (100–300 mg/L) of azo dyes was applied to decolorize Direct Blue
151 (DB151) and Direct Red 31 (DR 31). Carbon and nitrogen sources are given
to the bacterium as food, and growth was with required pH and temperature. They
observed that bacterium consortium was very effective for decolorization of azo
dyes and the effect was more pronounced when sucrose and yeast extract was
given as carbon and nitrogen source to bacterium. Biodegradation ability of
halotolerant bacteria was evaluated by Nicholson and Fathepure (2004) under
aerobic conditions. For this purpose, culture of halophilic bacteria dominated by
Marinobacter spp. was used to assess its potential to degrade benzene,
ethylbenzene, and toluene and xylene compound. It has been observed that this
bacterial culture completely degraded benzene, ethylbenzene, toluene, and
xylenes. The culture also mineralized the benzene that was evident from
conversion of (14C) benzene to (14CO2). They reported that activity of culture was
enhanced markedly by the addition of yeast extract as a growth-promoting
nutrient. Similarly, the ability of a halophilic archaea to degrade aromatic
hydrocarbons and a wide range of n-alkanes in the presence of salinity have been
documented by Oren et al. (1992) and Bertrand et al. (1990).
Feng et al. (2014) isolated salt-tolerant strain Pichia Kudriavzevii, and the
effect of salinity, initial concentration of azo dye acid red B, temperature, and pH
on decolorization performance of this strain was evaluated. On the basis of results,
they concluded that degradation efficiency of this strain was more than 94% and
optimal condition for its performance were salinity, 10%; initial concentration of
acid red B
solutions,100 mg/L; temperature, 33 ○C; and pH, 5.0. Asad et al. (2007) observed
that among 27 strains of halotolerant bacteria, 3 showed remarkable ability to
decolorize the azo dyes at various concentrations of NaCl and a wide range of pH
and temperature. These strains have potential to decolorize a pure as well as
mixture of dyes. They suggested that the decolorization was due to degradation
that was the result of reduction of azo bonds.
Polycyclic aromatic hydrocarbons cause harmful impact in aquatic environment
due to their carcinogenic nature in marine organisms (Perugini et al. 2007). Due to
their hydrophobic nature, these compounds can be adsorbed on a particulate
matter, and marine sediments act as sinks for such compounds (Yu et al. 2005;
Osuji and Ezebuiro 2006). Biodegradation of polycyclic aromatic hydrocarbon
such as naph- thalene, fluorene, anthracene, and phenanthrene by a halotolerant
bacterial consortium consisting of Ochrobactrum sp., Enterobacter cloacae, and
Stenotrophomonas maltophilia was studied by Arulazhagan et al. (2010). Various
concentrations of PAHs, i.e., 5, 10, 20, 50, and 100 ppm and a high level of NaCl
(30 g/L), were used to assess the degradation potential of the consortium. The
study showed that consortium degrades the PAHs within 4 days, and addition of
yeast extract further enhanced the degradation.
Sowmya et al. (2014) isolated 35 halophilic bacterial strains and categorized
these strains into moderately and extremely halotolerant. The isolated halophilic
bacterial strains were tested against lead and cadmium. The strains showed more
tolerance against lead than cadmium. And this tolerance was dependent on salt
concentration of the medium. Removal efficiency of selected isolates regarding
heavy metals showed that a maximum reduction of cadmium was less than lead,
i.e., 37 and 99%, respectively. They demonstrated that variable response of strains
were due to the toxicity of metals to strains and variable characteristics of two
strains. A positive response was observed when a fungus was used to remediate
petroleum- contaminated saline –alkaline soil (Qin et al. 2012). Zhang et al.
(2016) isolated salt-tolerant bacteria (Corynebacterium variabile). The isolated
bacterium with biochar as a carrier material was applied to see the bioremediation
potential of said strain. The bacteria caused significant effect on degradation of n-
alkanes and polycyclic aromatic hydrocarbons. Similarly, bioremediation
potential of halotolerant fungus Embellisia phragmospora was studied by Jenab et
al. (2016) against crude oil and pyrene. The strain was able to degrade 77, 83.4,
and 77.4% of petroleum at salinity of 0, 2.5, and 5%, respectively, during 7 days,
whereas pyrene removal was 82.4, 88.3, and 95.2% at these salinity levels.
The above-discussed review showed that in addition to improving plant growth
under salinity stress conditions, the halotolerant microbes are also successfully
used to remediate the contaminated environment. These microbes have a wide
range of characteristics that enable them to decontaminate the variety of soil
contaminants. Owing to their environment-friendly traits and less cost, these
microbes could be a suitable inoculum for their use on commercial basis.
10.6 Concluding Remarks and Future Prospectus
The above-discussed review showed that plants and microbes both are affected by
the harmful effect of salinity. Most of the studies reported in the literature indicate
that microbes have developed special mechanisms that enable them to survive and
grow in saline environment. Although the plants itself have defense mechanisms
against salinity, the interactions of plants with microbes further accelerate the
survival of plants in harsh environment. Owing to their number of growth
promotion mechanisms, these halotolerant microbes play a significant role in plant
tolerance against salinity. Lowering of stressed-induced ethylene by ACC-
deaminase, decreasing the Na availability by exopolysaccharides, enhancing the
activity antioxidant system, and producing osmolytes are the key traits which
dilute the negative effect of salinity, and plant showed better growth in saline
conditions. Symbiotic association of plant with these microbial strains enables the
plant to maintain growth by enhancing its capacity to produce compatible solute,
activity of antioxidant enzyme, nutrient acquisition, and water use efficiency. The
review mentioned in this chapter showed the significant positive impact of
microbial inoculation on plant, and it has been noted that inoculated plants were
more resistant to salinity. It has also observed that halotolerant microbes are
equally important to degrade harmful compounds present in contaminated
environment. These strains have competitive advantage over non-halotolerant
microbes due to their ability to cope with harsh environmental conditions and
presence of some particular traits that enable them to accelerate the process of
bioremediation effectively.
It has also observed from the literature that most of the work conducted under
axenic conditions with control environmental conditions. However, less work has
been done to evaluate the efficacy of these microbes in natural environment. For
the application of halotolerant bacteria as biofertilizers and bioremediation agents,
several aspects like its survival, optimum environmental conditions, and ability to
compete with indigenous population are still needed to be explored. Similarly,
instead of using single strain, the effectiveness of multi-strain inoculum is needed
to be evaluated in laboratory as well as in field. Also before using multi-strain
inoculum, their compatibility with each other needs to be tested so that maximum
benefits can be obtained. The application of halotolerant microbes in the field of
biotechnology is another area that requires special attention so that maximum
benefits can be obtained from this naturally occurring population.
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Manoj Kumar · Hassan

Etesami Vivek Kumar

ISBN 978-981-13-8334-2 ISBN 978-981-13-8335-9 (eBook)

Ranchi, India Manoj Kumar

1 Soil Salinity as a Challenge for Sustainable Agriculture and

8 Production of Rhamnolipids by a Halotolerant Bacterial

Manoj Kumar is an Associate Professor at the Depart-

Hassan Etesami is a Research Scientist with 10 years

His research areas include microbial ecology,

Vivek Kumar is an Associate Professor, involved in

Hassan Etesami and Fatemeh Noori

# Springer Nature Singapore Pte Ltd. 2019 1

available in a shorter time frame. Such inoculants contribute to the development

1.2 Salinity Effect on Growth of Plants and Mechanisms

susceptibility to diseases), and decrease in photosynthetic activity (Arbona et al.

1.3 Bacterial-Mediated Alleviation of Salinity Stress in Crop

Plant-associated beneﬁcial microorganisms including rhizoplane, rhizosphere and

1.3.1 Mechanisms of Action by Which PGPR Alleviate Salt Stress

Halotolerant PGPR including Azospirillum, Rhizobium, Bacillus, Pseudomonas,

Table 1.1 (continued)

Kucharova 2009; Mantelin and Touraine 2004). For example, IAA-

(catalase), GPX (glutathione peroxidase), SOD (superoxide dismutase),

The microbial communities inhabiting the rhizosphere of halophytic plants, also

competence by beneﬁcial bacteria. In: Bacterial metabolites in sustainable agroecosystem.

Paul D, Anandaraj M, Kumar A, Sarma YR (2005) Antagonistic mechanisms of ﬂuorescent

Leila Bensidhoum, Sylia Ait Bessai, and Elhafid Nabti

L. Bensidhoum · S. Ait Bessai · E. Nabti (*)

# Springer Nature Singapore Pte Ltd. 2019 23

The rapidly increasing human population is causing a number of challenges to

2.2 Salinity and Salinization

Soil salinization consists of water-soluble salt accumulation in soil that includes

Additionally, about one-third of the world’s irrigated lands contributing with

2.3 Effects of Salinity on Soil, Plants, and Microorganisms

2.3.1 Effect on Soil Quality

2.3.2 Effect on Plant Growth Activities

Salinity constitutes a most critical constraint, which hinders and causes a

Many studies have demonstrated that salinity inhibits seed germination of

2.3.3 Effect on Rhizospheric Bacteria

of organisms are permeable to water but not to other metabolites. Therefore,

2.4 Halotolerant PGPRs as a New Strategy to Alleviate

Table 2.1 Salinity stress alleviation by PGPR species in various crops

2.4.1 Mechanisms of Plant Promotion by Halotolerant

Potential of halotolerant PGPRs to increase crop productivity under stressful envi-

2.4.1.1 1-Aminocyclopropane-1-carboxylic Acid (ACC) Deaminase

2.4.1.2 Phytohormone Biosynthesis

2.4.1.3 Induced Systemic Tolerance (IST): Antioxidant Enzymes

uninoculated non-stressed plants. Plants’ salt-stressed roots inoculated with

2.4.1.4 Ion Homeostasis and Nutrient Uptake

2.4.1.5 Osmoprotective Compounds: Compatible Solutes

2.5 Halotolerant PGPR Algae: A Promising

Improvement of plant growth in saline soils by inoculation with halotolerant

Sandhya V, Ali S, Grover M, Reddy G, Venkateswarlu B (2009) Alleviation of drought stress

Siddikee MA, Chauhan PS, Anandham R, Gwang-Hyun H, Tongmin S (2010) Isolation,

Vacheron J, Desbrosses G, Bouffaud ML, Touraine B, Moënne-Loccoz Y, Muller D, Legendre

A. Alexander · A. Mishra (*) · B. Jha (*)

# Springer Nature Singapore Pte Ltd. 2019 53

As human probiotics, plant-probiotic microorganisms (PPM) are beneﬁcial

3.2 Effect of Salt on Plant Growth

3.2.1 Osmotic Stress

A. Alexander · A. Mishra () · B. Jha ()