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Legume-based intercropping systems promote beneficial rhizobacterial

community and crop yield under stressing conditions

Article in Industrial Crops and Products · September 2022

DOI: 10.1016/j.indcrop.2022.114958

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 Industrial Crops & Products 183 (2022) 114958

Contents lists available at ScienceDirect

Industrial Crops & Products

journal homepage: www.elsevier.com/locate/indcrop

Legume-based intercropping systems promote beneficial rhizobacterial

community and crop yield under stressing conditions
Imane Chamkhi a, *, Said Cheto a, b, Joerg Geistlinger c, Youssef Zeroual d, Lamfeddal Kouisni e,
Adnane Bargaz a, Cherki Ghoulam a, b, **
a
Mohammed VI Polytechnic University, Agrobiosciences, Plant & Soil Microbiome Subprogram, Bengurir, 43150, Morocco
b
Cadi Ayyad University, Centre of Agrobiotechnologie & Bioengineering, Research Unit Labeled CNRST, Faculty of Sciences and Techniques, PO Box 549, Gueliz,
Marrakech, Morocco
c
Anhalt University of Applied Sciences, Bernburg, Germany
d
Situation Innovation-OCP group, Jorf Lasfar, Morocco
e
African Sustainable Agriculture Research Institute (ASARI), Mohammed VI Polytechnic University (UM6P), 70000, Foum El Oued, Laayoune, Morocco

A R T I C L E I N F O A B S T R A C T

Keywords: Intercropping is an adapted farming system to optimize resource-use efficiency and crop yield, particularly in low
Legume-based intercropping input agricultural systems. Due to the beneficial eco-agricultural effects of grain legumes, their integration in
Rhizosphere mixed cropping systems such as intercropping systems can be more beneficial to soil fertility, soil functioning,
Bacterial community composition
and nutrient cycling. About 16–22% of the world’s food is provided by cropping systems. On smallholder farms
PGPR
Stress tolerance
in Eastern and Southern Africa, the integration of legumes has the potential to increase maize (Zea mays) pro­
duction up to 35% (e.g., Maize-pigeon pea (Cajanus cajan) intercropping). Legume-based intercropping systems
can also promote rhizobacterial community diversity and soil health by enhancing symbiotic and non-symbiotic
beneficial population. In the rhizosphere, the bacterial community is required to improve the growth and health
of both intercrops due to several “direct and indirect” mechanisms involving plant growth-promoting rhizo­
bacteria (PGPR). This review aims to highlight the importance of both legume-based intercropping and root-
associated microorganisms particular emphasis on rhizobacteria; since the whole “crop-crop-microorganism”
system has the potential to improve crop agro-physiological performance. This study also discusses the key role
of legumes as intercrops being fully synergistic with PGPR contributing to crop yield stability under stressful
conditions, notably drought and nutrient deficiency. Thus, intercropping can be used as an agroecological
practice to ensure the sustainability of production.

1. Introduction these have revealed the interest of intercropping systems to minimize

the effects of abiotic stresses on crop productivity (Tsubo et al., 2005;
Productive agro-systems depend on several factors, including fertil­ Asgharipour and Rafiei, 2010; Layek et al., 2018).
ization regimes (Cuvardic et al., 2004), plantation types (Hartemink, Intercropping is an ancient agricultural practice of mixed cropping
2005), cropping systems (Obasi et al., 2013), and other biotic and that involves planting two or more crop species together in the same
abiotic factors (Pandey et al., 2017). Abiotic stresses are the major space and at the same time (Massawe et al., 2016; Dai et al., 2019). The
limiting factors that influence soil ecosystem and agricultural produc­ most common combination for this practice is legumes/cereals (Layek
tivity (Kumar et al., 2020), notably drought, low and high temperatures, et al., 2018). According to the meta-analysis study by Tang et al. (2021)
salinity, and nutrient deficiencies. All of these factors are deleterious in on the efficiency of using phosphorus (P) in cereal/legume intercrops, a
influencing plant defense and physiological responses (Pandey et al., significant increase in the absorption of P and the equivalent ratio-soil
2017). Current investigations showed that some innovative agricultural for P uptake (averaged 1.24) was observed, while the net effect for P
practices can mitigate the impacts of stress on crops. Some studies of uptake was 3.67±1.00 kg ha-1 and the absolute gain of P uptake due to

* Corresponding author.
** Corresponding author at: Mohammed VI Polytechnic University, Agrobiosciences, Plant & Soil Microbiome Subprogram, Bengurir 43150, Morocco.
E-mail addresses: [email protected] (I. Chamkhi), [email protected], [email protected] (C. Ghoulam).

https://doi.org/10.1016/j.indcrop.2022.114958
Received 28 December 2021; Received in revised form 12 April 2022; Accepted 14 April 2022
Available online 26 April 2022
0926-6690/© 2022 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).
I. Chamkhi et al. Industrial Crops & Products 183 (2022) 114958

intercropping increased to 6.87 kg ha-1; showing a high use of P while information generated by this review could be useful for the imple­
reducing the need for P fertilizer in intercrops than in sole crops for the mentation of sustainable agricultural practices through the combination
same yields. of microbial inoculants as environmentally friendly biofertilizers and/or
Furthermore, the integration of legumes of particular interest to biostimulants and the legume-based intercropping system as key agri­
staple cereal crops such as maize or wheat (Triticum aestivum), which are cultural practices with the potential to thrive under stressful conditions.
a key crop for food security, can improve yields through use of soil re­
sources. Practicing intercropping with legumes can improve the utili­ 2. Integration of legume crops into agricultural systems affects
zation of nutrient resources and subsequently improve the growth the biochemical and physical soil properties
performance of both intercrops for low-input farming systems (Tsubo
et al., 2005). Indeed, the highest maize yields were recorded in con­ Low soil fertility is a critical constraint for crop production and the
servation agriculture systems with groundnut (3609 kg ha− 1) and incorporation of legumes into cropping systems has shown improved
common bean (3307–3576 kg ha− 1) in rotation and intercropping physico- chemical-biological proprieties and soil fertility (Fig. 1).
(Mupangwa et al., 2021) indicating the contribution of legume in­ Therefore, there is a need to explore and optimize the use of legume-
tercrops to stabilize maize yields and more remarkably under environ­ intercropping systems to generate beneficial effects on soil nutrient
mental constraints (Dai et al., 2019). In vulnerable situations, this availability and use efficiency. Some studies on the effect of legumes
intercropping system has various benefits such as improving fertility by have revealed remarkable changes in soil chemical characteristics such
increasing nutrient availability and soil quality (Betencourt et al., 2012; as total nitrogen (N), pH, and organic carbon. The incorporation of le­
Bi et al., 2019), including water use efficiency likely to improve under gumes as a green manure significantly raised soil pH (Kiiya et al., 2010),
drought conditions (Yin et al., 2020). On the other hand, legume-based impacting soil acidification due to carbon (C) and N cycles, as reported
intercropping systems are known to ameliorate the relevance of micro­ by Burle et al. (1997).
bial diversity for soil functioning (Zhang et al., 2010). Moreover, in semi-arid areas, soil chemistry and fertility can be
In addition, the rhizobacteria diversity can enhance plant growth, affected by the incorporation of legumes, since the incorporation of
through their plant growth promoting (PGP) characteristics at the lablab, soybean (Glycine max), and mucuna (Mucuna pruriens) showed
rhizosphere where nutrients become more available for roots Chamkhi positive effects on soil chemical properties (Adesoji et al., 2014). In fact,
et al. (2021b)). Consequently, rhizobacterial (PGPR) population can act these legumes significantly increased soil organic carbon, soil available
as biofertilizers acting either directly or indirectly to benefit plant P, and soil total N, but significantly reduced exchangeable cations and
growth and development (Lian et al., 2019; Chamkhi et al., 2021b). soil C: N compared to the weedy fallow (Adesoji et al., 2014). According
These PGPR may act through their various beneficial roles in mineral to Cong et al. (2015), soil organic carbon content in the top 20 cm was
nutrient cycling, organic matter turnover, nitrification, mobilization, 4% higher in intercrops (maize with wheat or faba bean) than in sole
mineralization and the formation of soil structure essential in plant crops (maize, wheat and faba bean), indicating a difference of
growth (Panhwar et al., 2013). 184 kg ha− 1 yr− 1 in carbon sequestration rate between intercropping
This review aims to investigate the importance of legume crops, the and monoculture systems. In addition, soil organic N content in the top
agro-ecological services of intercropping with legumes and their benefits 20 cm was 11% higher in intercrops than in sole crops, indicating a
on soil properties and the functional diversity of the soil microbial difference in N sequestration rate between intercrop and sole crop sys­
community under stress conditions. In addition, the review highlights tems of 45 ± 10 kg N ha− 1 yr− 1 (Cong et al. (2015).
the PGPR actions, their positive role on plant growth, their interactions In terms of soil physical properties, the majority of legumes were
with intercropped leguminous and non-leguminous species. The found to improve bulk density, cone penetrometer resistance, saturated

Fig. 1. Schematic representation of legumes beneficial effects on soil properties.

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I. Chamkhi et al. Industrial Crops & Products 183 (2022) 114958

hydraulic conductivity, and cracking clay (Armstrong et al., 1999). Furthermore, the integration of legume crops as management op­
Moreover, under the legume intercropping system, the proportion of tions plays a central role in increasing effective rhizobia number in the
macro-and micro-aggregates was increased by 52% and 111%, soil (Thies et al., 1991) and influencing legume biomass with a high
compared to sole crops (Garland et al., 2017). Furthermore, this farming potential to positively affect net fixed nitrogen inputs (Peoples et al.,
practice impacts soil loss by erosion (Reddy et al., 1980). For instance, 1995; Stagnari et al., 2017) (Fig. 1).
sorghum-cowpea intercropping reduced runoff by 20–30% compared to
sorghum sole crop and by 45–55% compared to monocropped cowpea 3. Intercropping systems: legume-based intercropping
(50% reduced soil loss with intercropping) (Reddy et al., 1980).
Moreover, the integration of legumes such as faba bean (Vicia faba) Intercropping is the practice of growing two or more crops in the
(Song et al., 2007), Alfalfa (Medicago sativa) (Sun et al., 2009; Zhang same season on the same land (Lithourgidis et al., 2011). Compared to
et al., 2018), soybean (G. max) (Fu et al., 2019), pigeon pea (C. cajan), sole cropping systems, intercropping productivity has a great potential,
groundnuts (Arachis hypogaea), and cowpea (Vigna unguiculata/beans to substantially optimize cropping systems under limiting resources like
(Phaseolus vulgaris) (Mucheru-Muna et al., 2010) has been reported to light, water, and nutrients (Yin et al., 2020). Legume intercropping is a
have an impact on soil biological activities, especially through changes promising way to diversify crops and eco-intensify the production of
in microbial communities. Additionally, this integration affects soil cropping systems and can be used to enrich soils with biologically fixed
biological activities such as those related to arbuscular mycorrhizae N due to legume-rhizobia symbiosis, thereby improving the soil quality
(AM), but decreases also the amounts of plant-parasitic nematodes and soil organic carbon accumulation (Raji and Dörsch, 2020). In
(Alvey et al., 2001) and increases the microbial abundance in the addition, the mixture of two or more crop species like cereals and le­
rhizosphere (Zhang et al., 2010). Legume crops are a source of N in the gumes contrasting in terms of root systems and rhizosphere activities
field (Ghosh et al., 2007) through the atmospheric N fixed symbiotically often generates better cover and efficient soil exploration for better
following the interaction between legumes and rhizobia (Rhizobium spp) resource uptake (Layek et al., 2018) (Fig. 2). For instance, the most
(Peoples et al., 1995). Legume-based cropping, long known for its common intercropping combinations in cereal-legume systems, are
beneficial effects either in crop rotation system or intercropping system, maize (Z. mays)/ soybean (G. max) (Fu et al., 2019), maize
is a renewable source of N for crop production to improve the N balance (Z. mays)/pigeon pea (C. cajan), maize (Z. mays)/groundnuts (Arachis
in poor soils (Stagnari et al., 2017). hypogaea), maize (Z. mays)/cowpea (Vigna unguiculata), maize

Fig. 2. Roots systems of intercropped legume and cereal with different explored soil layers allowing complementarity while avoiding root-root competitiveness.

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I. Chamkhi et al. Industrial Crops & Products 183 (2022) 114958

(Z. mays)/beans (Phaseolus vulgaris) (Mucheru-Muna et al., 2010), mil­ intercrop micro-aggregates compared to sole maize (84 vs. 29 mg Pkg− 1,
let/groundnuts (Arachis hypogaea), sorghum/cowpea (Vigna unguiculata) respectively) (Garland et al., 2017). Biologically fixed N increased from
(Nyoki and Ndakidemi, 2016), rice (Oryza sativa) /pulses and barley 89% in the sole pigeon pea to 96% in the intercropping system (Garland
(Hordeum vulgare)/faba bean (V. faba) (Dwivedi et al., 2015; Mouradi et al., 2017). Additionally, cowpea-maize intercropping improved soil P
et al., 2018). It should be mentioned that several factors are involved in availability and maize yields in alkaline soils (Latati et al., 2014). Under
the performance of the intercropping system, such as the suitable cul­ P-deficient conditions in an intercropping system like soybean (G.max)
tivars, competition between crops and seeding ratio (Layek et al., 2018). and wheat (Triticum aestivum), this crop combination stimulates root
microbial diversity, root biomass allocation, and P-hydrolyzing acid
4. Advantages of intercropping with legumes under limiting phosphatases activity in roots. Consequently, increased microbial di­
conditions versity and root-induced morphological and biochemical changes
contribute to improving P and N acquisition (Bargaz et al., 2017). Ac­
Arid or dry agriculture lands under drought rainfed conditions, cording to Betencourt et al. (2012), the increased P availability in the
mainly in Africa (Van Duivenbooden et al., 2000), are fragile ecosystems rhizosphere was higher when the two species were intercropped (durum
suffering from various problems like scarcity of freshwater resources wheat and chickpea) compared to monoculture (durum wheat or
(Tanwar et al., 2014). Under such stressful conditions, legume-based chickpea). Such an increase could be a consequence of root-induced
intercropping has been reported to positively influence productivity alkalization as well as other root-induced processes e.g., exudation of
compared to sole cropping systems. In addition, increased resource use phosphatases, carboxylates. Meanwhile, in the rhizospheric soil of
could improve the growth performance of both intercrops, especially in barley intercropped with faba bean, an increase of available P content
situations of limited water resources (Bargaz et al., 2016) and/or was confirmed and coincided with an increase of acid phosphatase ac­
low-input farming system (Tsubo et al., 2005) through increased stress tivity (Mouradi et al., 2018).
tolerance and resource use efficiency (Fig. 2) (Yin et al., 2020). Indeed, In pea–barley intercropping systems, Corre-Hellou et al. (2011)
the increase in water use efficiency in legume/non-legume intercrop­ found that soil nitrogen availability was one of the main factors influ­
ping systems, compared to sole cropping, was attributed to comple­ encing intercropped species interactions. Low soil N availability was
mentary interactions for water uptake due to differences in root probably related to low water availability at several studied sites, partly
distribution across soil layers and decreasing evaporation loss through explaining the decline in pea growth with decreased soil N availability
better vegetative cover (Van Duivenbooden et al., 2000; Layek et al., (Hauggaard-Nielsen et al., 2001). In Argentinean, comparing the crops
2018). of sole corn (Zea mays L.), sole soybean (G. max L.), corn-soybean 1:1
On the other hand, legume-based intercropping systems not only intercropping and corn-soybean 1:2 intercropping, demonstrated that
induce rich soil organic matter with better capacity to conserve water in the practice of intercropping does not improve water uptake compared
the root zone for sufficient water supply, but also improve soil fertility to sole crops (Ariel et al., 2013). Corn N status was improved with
(Tirado and Cotter, 2010). Furthermore, as in the case of cereals (e.g., intercropping probably due to increased plant and root growth, but
millet and sorghum) intercropped with legumes (e.g., cowpea and soybean chlorophyll content was reduced by intercropping treatments
groundnut), the increased yields of these two crops have been attributed (Ariel et al., 2013).
to nutrient factors; such as higher levels of mineral N and P availability Overall, intercropping can contribute to multiple agro-ecosystem
for cereals/legumes (Alvey et al., 2001). Improving soil fertility and services by increasing yield, soil C sequestration, and improved soil
nutrients requires inexpensive organic fertilizers for resource-poor quality. Direct interspecific facilitation in intercropping involves below-
farmers. In sub-Saharan Africa (Malawi), gliricidia–maize intercrop­ ground processes in which cereals increase Fe and Zn bioavailability to
ping can be an appropriate option for improving soil fertility and the benefit of companion legumes (Xue et al., 2016).
increasing yields in highly populated areas. Application of gliricidia
prunings tripled maize yield (3.8 Mg ha− 1) compared to cropping sole 5. Intercropping with legume interaction on rhizobacterial
maize without any soil amendment (1.1 Mg ha− 1) (Makumba et al., interactions
2006).
However, according to Asgharipour and Rafiei (2010), lentil (Lens The rhizosphere is the soil area intimately related and influenced by
culinaris)/isabgol (Plantago ovata) intercropping system reduced the the plant roots and the microorganisms associated with them (Kuzyakov
impact of drought on plant productivity, significantly decreased inter­ and Razavi, 2019). Compounds secreted by plant roots attract a wide
crop growth (isabgol and lentil crops) and total N concentration of range of microbial associations (symbiotic interactions, mutualism,
isabgol plants. In addition, intercropping brings other positive effects commensalism, parasitism, and pathogenic interactions) (Badri et al.,
such as reducing the risk of single crop failure, increasing soil organic 2009; Uroz et al., 2019). Moreover, these compounds are able to interact
carbon content, diversifying farm income and reducing herbicide input with microbial receptors, thus inducing signaling pathways that coor­
(Asgharipour and Rafiei, 2010). dinate the interactions in the rhizosphere (Olanrewaju et al., 2019).
Healthy, nutrient-rich soil is an important and critical factor in Stimulation of microorganisms (Plant-microbe interaction) via plant
stressful conditions. The interaction of legumes in intercropping systems root exudates could have different results depending on the type of soil,
affects soil nutrient availability and soil biogeochemical cycling, which the microorganism involved, and the nature of the host plant (Chamkhi
enhances plant growth and tolerance to abiotic and biotic stresses (Dai et al., 2021a).
et al., 2019). Consequently, intercropping with legumes can be recom­ This dynamic is maintained and mobilized by continuous exchanges,
mended, in some cases, to small-scale farmers in the semi-arid zone which modify the physico-chemical-biological properties of the rhizo­
(Tsubo et al., 2003). spheric soil (Wei et al., 2019). Interactions between microbes and plants
The beneficial effects of legume/cereal intercropping on nutrient in the rhizosphere may result in either harmful or beneficial effects
availability and uptake have been widely documented mainly in the case (Pathan et al., 2020). These effects of microorganisms depend on several
of P. Thus, in pigeon pea intercropping with maize, the physical root factors such as the microbial strains involved, the plant species, the type
contact (rhizosphere) and their biochemical activities can have a posi­ of interaction (Jones and Hinsinger, 2008). Several microorganisms are
tive and significant impact on soil structure as well as nutrient storage in commonly used as biofertilizers, including N-fixing soil bacteria,
these high P-sorbing soils (Garland et al., 2017). Consequently, the N-fixing cyanobacteria, phosphate-solubilizing bacteria, phytohormone
proportion of macro- and micro-aggregates increased by 52% and 111%, (auxin)-producing bacteria, etc (Chamkhi et al., 2021b). Rhizobacterial
respectively, in the intercropping treatment compared to sole maize. associations are considered the most important within the rhizosphere.
Therefore, there was a significant increase in organic P storage in Unlike chemical fertilizers, biofertilizers are viable microorganisms that

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I. Chamkhi et al. Industrial Crops & Products 183 (2022) 114958

are not the source of nutrients but help plants access nutrient availability 2014). While the second group consists of free-living rhizobacteria that
in the rhizospheric area (Umesha et al., 2018; Kumar et al., 2020). live outside the cells, but they are also involved in improving yield
Moreover, PGPR inoculation is one of the strategies adopted to through their fertilizing effects (Hayat et al., 2010). This association is
improve sustainable agriculture cropping system, and advisable under very common in several plant species, which allows them to acquire
abiotic stresses due to their direct and indirect roles as biofertilizers, several phenotypes such as the assimilation of micronutrients and the
phyto-stimulants, and biopesticides (Goswami et al., 2016). PGPR accumulation of secondary metabolites (Aly et al., 2010; Datta et al.,
exhibit many beneficial properties such as phytohormone synthesis, 2020).
1-aminocyclopropane-1-carboxylate (ACC) deaminase and siderophore The growth-promoting rhizobacteria colonize the rhizosphere of
production, N fixation, P and potassium (K) solubilization, and the many plant species and confer beneficial effects on them due to their
organic osmotica synthesis that could ensure crop protection under important roles in biofertilization, rhizoremediation, biocontrol, and
stress conditions, thus improving production and its sustainability phytostimulation. PGPR strains can promote plant growth and devel­
(Kumar et al., 2020). The use of rhizobacterial inoculation under stress opment either directly and/or indirectly. Direct mechanisms include the
to boost the yield of intercrops is a promising tool in agricultural prac­ production of phytohormones (auxins, cytokinins, and gibberellins),
tice that suggests the possible use of these strains as environmentally enzymes (ACC-deaminase), mineralization of organic matter, increased
friendly solutions to ensure the healthy crop growth. P and K availability through solubilization of their relative insoluble
While the use of a single bacterial inoculum or bacterial consortia forms and the contribution to N nutrition via the biological N fixation
(consisting of two or more bacterial species living in association without process. While indirect mechanisms include production of antibiotics
any antagonism) as an effective inoculum on poor soils, can help in­ and siderophores (chelation of available Fe), induction of systemic
crease nutrient uptake efficiency (Panhwar et al., 2013; Xu et al., 2018). resistance, and hydrolysis of molecules released by pathogenic PGPR for
Thus, well-adapted and efficient rhizobacteria inocula could be selected biocontrol of plant diseases (Ortíz-Castro et al., 2009; Bhattacharyya
for a convenient low input farming system to cope with climate and Jha, 2012). Other PGP traits are summarized in Fig. 3.
change-induced abiotic stresses and ensure food security. In the rhizosphere, a close exchange exists between the plant and the
The rhizobacteria, as colonizing bacteria of the rhizosphere, provide rhizobacteria. In fact, plants can stimulate rhizobacteria by secreting
remarkable beneficial effects to host plants by stimulating their growth root exudates and phytochemical metabolites that engage the rhizo­
and enhancing their health. According to their location and their bacterial community to react with the plant (Vishwakarma et al., 2020).
tropism in relation to the host plants, PGPR are classified into two major In contrast, the rhizobacteria can also act on plants by releasing several
groups (Bais et al., 2006; Okon et al., 2015). The first group induce molecules particularly acylated homoserine lactones (AHL) and other
nodule formation and plant cell colonization (intracellular PGPR) lives quorum-sensing mediators (Chamkhi et al., 2020). In the particular case
in symbiosis with plants (Hayat et al., 2010). The representative bac­ of the legume-rhizobium interaction, the plant initiates this symbiotic
terium of this group is rhizobia-type bacteria that colonize certain interaction by the secretion of isoflavonoids and the bacterium responds
leguminous plants and fix N in their root nodules (Masciarelli et al., with a lipochitooligosaccharid (Nod factor) determining for the success

Fig. 3. Rhizobacteria modes of action. Rhizobacteria (symbiotic or free-living) can influence plant growth through several mechanisms including growth enhancement, N
fixaxtion, production of growth regulators, and resistance against abiotic and biotic stress.

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I. Chamkhi et al. Industrial Crops & Products 183 (2022) 114958

of symbiosis establishment. This communication represents the first step intercropping systems can affect the composition of soil rhizosphere
by which plants selectively and specifically target colonizing bacterial bacterial communities (Table 1).
populations. Through a variety of molecules, the plant can also control In fact, intercropping with legumes improves soil properties by
the expression of rhizobacteria genes responsible for several functions enhancing the functional diversity of the soil microbial community
(Fig. 4), particularly those making nutrients more available by chelating therefore improving plant growth. Clearly, soil microbial community is
and transporting them to plants, producing phytohormones, antibiotics, important for soil functions, due to its roles in mineral nutrient cycling,
and secondary metabolites, inducing mobility, and inhibiting biofilm organic matter turnover, nitrification, mobilization, mineralization and
formation (Chamkhi et al., 2021a; Pascale et al., 2020). soil structure formation that are essential for plant growth (Panhwar
On the other hand, the chemotaxis of PGPR and the behavior of root- et al., 2013). Therefore, changes in ammonia-oxidizing bacteria (AOB)
associated bacteria are influenced by crop association, a consequence of or archaea (AOA) community structure could potentially affect impor­
the changes in the composition of root exudates that play a distinct role tant soil processes, such as nitrification, as found in wheat/faba bean,
in the physiological ecology of plant beneficial bacteria. In intercrop­ wheat/maize, maize/faba bean rhizosphere (Zhang et al., 2015; Xu
ping of legumes (pigeon pea) and cereals (maize), it has been shown that et al., 2018). On the other hand, changes in the community structure
a cross-migration of bacteria from the roots of one plant to another can have been shown to have functional significance for processes such as
occur on the roots of the companion plant even if it was not inoculated soil P and C cycling, through microbial biomass phosphorus (MBP) and
(Vora et al., 2021). microbial biomass carbon (MBC) changes in the rhizosphere (Tang et al.,
2014). In intercropped durum wheat/chickpea and durum wheat/lentil
6. Soil bacterial community diversity under legume rhizosphere, CMB was reported to be increased in the rhizosphere only
intercropping systems for the intercropped plants. Similarly, an increase in P availability in the
rhizosphere was recorded in response to intercropping in one of three
Microbial community composition in the soil is influenced by several crop species (Tang et al., 2014). Furthermore, Yang et al. (2019)
factors such as environmental parameters, fertilization, pesticides, and demonstrated that intercropping with legumes generally improves crop
agriculture practices (García-Orenes et al., 2013; Prashar and Shah, productivity by increasing N-fixing bacteria (Chen et al., 2018) or the
2016). Variance partition analysis showed that planting patterns abundance and composition of the diazotrophic community like Bra­
contributed to 26.7% of the total bacterial community variation (Zhang dyrhizobium and Skermanella that were the two dominant diazotrophic
et al., 2018). Moreover, plant species could affect the composition of soil genera identified in oat rhizosphere soil samples under the intercropping
rhizosphere bacterial communities (Rooney and Clipson, 2008). system (Yang et al., 2019).
Numerous investigations have focused on the diversity of soil bac­ As detailed in Table 1, the bacterial community compositions re­
terial communities in legume intercropping systems (Table1). The mo­ ported in many intercropped legume surveys were summarized. These
lecular approaches allowed the identification of a remarkable diversity studies were conducted to examine the rhizobacterial population under
of soil bacterial under legume intercropping systems (Fig. 5). intercropping with legume. As can be seen, through different molecular
Thus, many previous studies showed that cereal/legume methods, the intercropping field demonstrates a richness in the bacterial

Fig. 4. Schema represents some molecular ex­

change between roots plant and the bacteria
(plant-bacteria interactions) in the rhizosphere.
Plant roots secrete exudates and phytochemicals
molecules that stimulate the rhizobacterial com­
munity to coexist with the plant (plant beneficial
actions to rhizobacteria). In turn the rhizospheric
bacteria produce signal molecules such as N-acyl
homoserine lactone (AHL), volatile organic com­
pounds (VOC) and quorum sensing (QS) to
communicate and ensure rhizobacteria beneficial
actions to plants.

6
I. Chamkhi et al. Industrial Crops & Products 183 (2022) 114958

Fig. 5. Shema represents the experimental design of the metagenomic analysis process to study the diversity of soil bacterial communities.

composition and crop species had obvious effects on bacteria commu­ Relative abundance was significantly higher in intercrops with legumes
nity diversity in the rhizosphere soils. Comparing intercropping and (Sun et al., 2009; Zhang et al., 2018; Tang et al., 2014; Yang et al., 2016,
monocropping, the rhizobacterial composition was similar at the taxo­ 2019; Cao et al., 2017; Li and Wu, 2018; Li et al., 2018; Chen et al., 2018;
nomic level of phylum, but the relative abundances were different. Fu et al., 2019; Gong et al., 2019). As summarized in Table 1, all of the

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I. Chamkhi et al. Industrial Crops & Products 183 (2022) 114958

Table 1 Table 1 (continued )

Some investigations of rhizobacterial diversity under legume-based intercrop­ Intercropped Molecular Bacterial composition References
ping systems. plant species identification
Intercropped Molecular Bacterial composition References method or
plant species identification Sequencing
method or method
Sequencing Broomcorn millet Illumina MiSeq Actinobacteria, (Cao et al.,
method (Panicum sequencing Bacteroidetes, 2017)
Maize (Zea Illumina MiSeq Proteobacteria, (Fu et al., miliaceum) /red Proteobacteria,
mays)/ Soybean sequencing Chloroflexi, 2019) kidney bean Acidobacteria,
(Glycine max) Acidobacteria, (Phaseolus Gemmatimonadetes,
Actinobacteria, vulgaris) Chloroflexi,
Gemmatimonadetes, Broomcorn Planctomycetes,
Planctomycetes millet/red
Gemmatimonadetes, adzuki bean
Planctomycetes, (Vigna
Firmicutes, angularis)
Bacteroidetes, Broomcorn
Verrucomicrobia, millet/soybean
Nitrospirae, (G. max)
Saccharibacteria, Peanut PCR-Denaturing Gemmatimonasaurantiaca, (Yang
Latescibacteria, (A. hypogaea)/ Gradient Gel Flavobacterium, et al.,
Cyanobacteria Buckwheat Electrophoresis uncultured Acidobacteria 2016)
Proso millet Illumina MiSeq Actinobacteria, (Gong (Fagopyrum (DGGE) bacterium,
(Panicum sequencing Proteobacteria, et al., esculentum) uncultured
miliaceum L.) / Chloroflexi, 2019) Peanut/ Gemmatimonadetes,
Mung bean Gemmatimonadetes, Glutinous uncultured bacterium,
(Vigna radiata) Acidobacteria, millet uncultured Flavisolibacter,
Nitrospirae, Peanut Luteibacter,
Firmicutes /Sorghum rhizovicinus,
Oat (Avena sativa) Illumina MiSeq Azohydromonas, (Yang (Sorghum Acidovorax,
/soybean sequencing. Bradyrhizobium et al., bicolor) Asticcacaulisexcentricus,
(G. max) Skermanella 2019) Peanut / Foxtail uncultured soil bacterium,
Oat/mung bean millet uncultured Chloroflexi
(V. radiata) Pseudomonas libanensis,
Alfalfa (Medicago Illumina MiSeq Proteobacteria, (Li and uncultured
sativa L.)/ sequencing Actinobacteria, Wu, 2018) delta proteobacterium,
cucumber Chloroflexi, Pseudomonas fulva,
(Cucumis Firmicutes,Acidobacteria, uncultured bacterium
sativus) Bacteroidetes, Sole-cropping: 16 S rDNA Gemmatimonas aurantiaca
Trifolium Gemmatimonadetes, glutinous millet sequencing and Flavobacterium.
(Trifolium Saccharibacteria, (Panicum Pseudomonas fulva.
repens L.) Cyanobacteria, miliaceum) Empedobacter brevis
/cucumber Planctomycetes, Sole-cropping:
Verrucomicrobia, sorghum
Nitrospirae, (S. bicolor
Latescibacteria, Moench)
Parcubacteria. Sole-cropping:
Maize (Z. mays) Terminal α-Proteobacteria,β- (Li et al., carrot
/Peanut Restriction Proteobacteria, Firmicutes, 2018) Maize (Z. mays) T-RFLP analysis Total bacteria, (Zhang
(Arachis Fragment Length Actinobacteria /faba bean Real-time total archaea, et al.,
hypogaea) Polymorphism (T- Bacillus, (V. faba) quantitative PCR Ammonia-oxidizing 2015)
RFLP) Analysis Burkholderia, (qPCR) assay bacteria
Pseudomonas, Archaea
Rhizobium. Maize (Z. mays)/ Terminal Proteobacteria, (Zhang
Wheat (Triticum Real-Time PCR ammonia-oxidizing (Xu et al., faba bean restriction Acidobacteria, Chloroflexi, et al.,
aestivum) /Faba bacteria 2018) (V. faba) fragment length Gemmatimonadetes, 2010)
Bean (Vicia ammonia-oxidizing polymorphism (T- Bacteroidetes,
faba) archaea RFLP) Actinobacteria,
Maize (Z. mays)/ T-RFLP technique Actinobacteria, (Chen Amplified 16 S Verrucomicribia,
Peanut Bacteroidetes, et al., rDNA restriction Firmicutes,
(A. hypogaea) Chlorophyta, 2018) analysis (ARDRA) Planctomycetes,
Cyanophyta, 16 S rDNA Sanger
Firmicutes, sequencing
Fusobacteria, Siberian wild rye Terminal Alphaproteobacteria, (Sun et al.,
Nitrospira, (Elymus restriction Betaproteobacteria, 2009)
Planctomycetes, sibiricus) fragment Length Gammaproteobacteria,
Proteobacteria. /Alfalfa polymorphism (T- Deltaproteobacteria,
Mulberry (Morus Illumina MiSeq Proteobacteria, (Zhang (M. sativa) RFLP) analysis Firmicutes, Actinobacteria
alba L.)/ alfalfa sequencing Acidobacteria, et al., Bacteroidetes
(M. sativa L.) Actinobacteria, 2018) Wheat Illumina MiSeq bacterial ammonia (Song
Gemmatimonadetes, (T. aestivum) sequencing oxidizers et al.,
Chloroflexi, /faba bean 2007)
Planctomycetes, (V. faba),
Bacteroidetes, Wheat/maize
Nitrospirae. (Z. mays),
Maize /faba
bean

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I. Chamkhi et al. Industrial Crops & Products 183 (2022) 114958

dominant bacterial phyla (Actinobacteria, Proteobacteria, Chloroflexi, AOA and nitrite-oxidizing bacteria (NOB). The legume-based inter­
Gemmatimonadetes, Acidobacteria, Nitrospirae, and Firmicutes) were cropping could significantly improve the abundance of AOA and AOB
markedly affected by intercropping patterns and common to the ma­ and also change the structure of soil microbes (Song et al., 2007; Zhang
jority of intercropping based legume (Maize /Soybean, Proso millet et al., 2015; Xu et al., 2018). Conclusively, intercropping inoculation of
(Panicum miliaceum L.) /Mung bean (Vigna radiata), Alfalfa (M. sativa rhizobium significantly increased the abundance of total bacteria, total
L.)/ cucumber (Cucumis sativus), Trifolium (Trifolium repens L.) /cu­ archaea, AOB, and AOA, which may decrease the nitrification in the
cumber, Maize/Peanut (Arachis hypogaea), etc). However, the rhizosphere.
sequencing of some different bacterial species was only present in Certainly, intercropping with legume as an agricultural practice is
monoculture crops, revealing the presence of Gemmatimonas aurantiaca, suggested to provide an effective tool to optimize the beneficial rhizo­
Flavobacterium sp, Pseudomonas fulva, and Empedobacter brevis (Yang bacterial colonization and services in the soil or the use of the bacterial
et al., 2016) (Table 1). inoculum in the perspective to consider it as an alternative to chemical
Furthermore, it is important to emphasize that the most dominant fertilizers.
rhizobacterial group in the intercropped legume soil was the Actino­
bacteria. These groups of bacteria have been reported to constitute a 7. Interactive mechanisms between legumes and non-legumes
group of important plant-associated spore-forming bacteria, which have and rhizobial strains
been studied for their biocontrol, plant growth promotion, and benefi­
cial interaction with plants (Palaniyandi et al., 2013). Under limiting The legume integration in the cropping system is recognized with
conditions, Actinobacteria group can enhance and promote plant growth different advantages in soil dynamics. During intercropping there is
as drought-tolerant bacteria under water-stressed conditions (Yandigeri close physical root proximity between legumes and non-legumes, these
et al., 2012). Furthermore, due to their abilities to treat plant diseases facilitative interactions can result in mixing of microbial communities of
and control pests and pathogens, PGP actinobacteria can be used as the two plant species when intercropped. Cross-migration of bacteria
biological options for crop protection and production (Palaniyandi et al., from the roots of one plant to others can occur within 28 days of sowing
2013; Sathya et al., 2017). (Vora et al., 2021). The major advantage is their ability to establish
Nitrification is an important process in the global N cycle. The mi­ symbioses with rhizobia that allow them to fix atmospheric N in
croorganisms involved in the nitrification process are mainly AOB or specialized structures (nodules) (Coba de la Peña et al., 2018). Under

Fig. 6. Interactive mechanisms between le­

gumes and non-legumes and rhizobial strains.
Low N levels induce legume roots to produce fla­
vonoids that stimulate rhizosphere-associated
rhizobia to produce Lipo chitooligosaccharides
(LCOs). Theselatter induce the development of
the nodule that increases the N levels and the­
acquisition of the resources that impacts posi­
tively the development of theroot. Consequently,
influences plant growth (shoots development,
photosynthesis, plant genotype, and chemical
compounds).

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I. Chamkhi et al. Industrial Crops & Products 183 (2022) 114958

limiting conditions, such as low soil N levels, the legume roots produce showed this capacity to enhance salinity stress tolerance in okra (Abel­
flavonoids. The release of these compounds in intercrops, both in le­ moschus esculentus) through the activation of reactive oxygen species
gumes and cereals, could impact the behavior of root-associated bacteria (ROS)-scavenging enzymatic activity. In addition, these rhizobacteria
(Li et al., 2016), and could also act as a chemo-attractant to concentrate increased the germination percentage and chlorophyll content of okra
the compatible rhizobium at the root surface (Abdel-Lateif et al., 2012), (Carlson et al., 2020). These phenotypes involved an up-regulation of
and stimulate rhizosphere-associated rhizobia to produce molecules involved in ROS signaling pathways (Habib et al., 2016).
lipo-chitooligosacharide. This latter induces a signaling cascade that Also, PGPR through several physiological, biochemical, and molec­
regulates the expression of symbiotic genes to relay the ular properties are able to induce systemic tolerance in plants against
rhizobia-mediated signal that ultimately initiates nodule development water stress. There is the induction of several phenotypes such as the
(Concha and Doerner, 2020). Then, produced nodules can positively osmotic adjustment, increased antioxidant metabolism, improved root
influence the N levels in the rhizosphere that will be, at least partially, growth and architecture, upregulation of phytohormones (auxin, cyto­
available for cereals (Fig. 6). Faba bean and wheat intercropping has kinin.), activation of phytohormone expression (jasmonic and salicylic
been shown to increase nodulation biomass due to four types of flavo­ acid), production of signaling molecules (e.g., sphingosine and psycho­
noids namely flavonol, isoflavone, chalcone, and hesperetin which have sine) and stress metabolites like glutamic acid, proline, and choline
been shown in legume root exudates promoted by wheat compared to (Carlson et al., 2020). Additionally, PGPR can improve ROS detoxifi­
monocropping (Liu et al., 2017). cation and induction of hormonal stress adaptations to alleviate cold
Interestingly, PGPR exhibited significant chemotaxis towards inter­ stress in plants (Moradtalab et al., 2020).
cropped root exudates. Consequently, biofilm formation and coloniza­ Water stress is a serious constraint to plant growth and development.
tion were better on intercropped plants (Vora et al., 2021). This suggests Managing this constraint is a strategy for crop success and in particular
that the legume and non-legume interaction with the PGPR in inter­ for stabilizing yields. It has been shown that certain rhizobacteria such
cropping systems promotes favorable exchanges between two crops that as Bacillus megaterium positively regulate water capacity of corn, in
positively impact their growth. particular the opening of the stomata, through the regulation of hy­
draulic conductivity and transpiration. Improved root hydraulic
8. Managing adapted rhizobacterial consortia and legume-based conductance was correlated with the expression of genes encoding the
intercropping systems to enhance plant growth under stressing ZmPIP protein (Zea mays plasma membrane intrinsic proteins) and PIP2
conditions (plasma membrane type two) aquaporin amount in their roots under salt
stress conditions (Marulanda et al., 2010).
8.1. The actions of rhizobacterial communities in plant tolerance to Furthermore, certain rhizobacteria (PGPR) increase osmolytes and
abiotic stresses activate some phytohormone pathways, which overcomes osmotic
shock in Arabidopsis thaliana (Chen et al., 2007). This mechanism has
Abiotic factors such as the salinity stress represent critical environ­ been linked to increased expression of proline which confers resistance
mental constraints limiting plant growth and development. Rhizoshpe­ to salt stress (Chen et al., 2007). In vitro experiments showed that
ric microorganisms, in particular rhizobacteria, are endowed with the inoculation of rice (Oryza sativa) plants under hydroponic and soil
propriety of resistance to salt stress (Goswami and Deka, 2020). Rhi­ conditions exposed to salinity by salt tolerant Bacillus amyloliquefaciens
zobacteria colonizing the rhizosphere play an important role in the was very sensitive and significantly improved plant growth and stress
growth and fitness of their plant hosts. Although under stress and tolerance of this plant species through the expression of at least 14 genes
nutritional limitations, these bacteria also confer several phenotypes under these conditions (Nautiyal et al., 2013). This bacterium activates
that may be beneficial to these plants (Buée et al., 2009). the expression of certain protein genes such as EREBP (Ethyl­
Colonizing rhizobacteria exhibit PGP activities such as P solubiliza­ ene-responsive element binding protein) an ethylene-sensitive protein,
tion, N fixation, production of hydrogen cyanide and ACC-deaminase SERK1 (somatic embryogenesis receptor-like kinase 1) a somatic embryo­
enzyme, as well as indole 3-acetic acid and siderophore, that are rela­ genesis receptor-like kinase, and NADP NADP-ME2 (malic enzyme)
tively common features of PGPR helping plants resist the most common which positively regulates salt stress tolerance (Nautiyal et al., 2013).
abiotic stresses (Kumar et al., 2019), such as soil nutrient deficiency, The mechanisms of plant tolerance to osmotic stress conferred by
salinity and drought stresses. In this field, several studies have suggested rhizobacteria are also linked to the regulation of ionic homeostasis.
that these bacteria could ensure this resistance via rhizospheric in­ Obviously, PGPR considerably reduce the concentration of NaCl by their
teractions. These research works were able to show that plants inter­ root release by increasing the transport affinities involved. This toler­
acting with halotolerant rhizobacteria develop a tolerance to soil salinity ance to salt stress is also accompanied by a modification of the pH via
(Shukla et al., 2012; Nautiyal et al., 2013). Many halotolerant rhizo­ organic secretion (Dodd and Pérez-Alfocea, 2012; Lugtenberg et al.,
bacteria are known today, including several species such as Zhinguel­ 2013). This mechanism was observed in maize inoculated with the
liuella, Agrobacterium tumefaciens, Brachybacterium saurashtrense, Vibrio, bacterial strain Azotobacter chroococcum. Furthermore, this inoculation
Brevibacterium casei, Bacillus amyloliquefaciens, and Haererohalobacter increased the levels of proline, chlorophyll, and phenolic compounds
(Shukla et al., 2012; Nautiyal et al., 2013). The molecular mechanisms (Rojas-Tapias et al., 2012).
by which these PGPR induce stress tolerance remain poorly understood.
However, the induction and transcriptional activation of several genes 8.2. The efficiency of bacterial consortia in the case of legume/cereal
that confer this resistance appear to be the underlying mechanism. By intercrops
expressing these phenotypes, plants increase chlorophyll content,
accumulate certain amino acids, especially proline, and stimulate the Currently, researchers are interested in exploring biological solutions
osmoprotector. All these mechanisms lead to a remarkable reduction in to address limitations in nutrient availability to enhance plant devel­
the effects of salinity. Indeed, rhizobacteria upregulate genes affected by opment away from chemical solutions. Therefore, the use of microbial
soil salinity, including proteins involved in membrane permeability and fertilizers is one of the most attractive choices. Microbes with different
integrity. It has been shown experimentally that the inoculation of attributes can be used as bio-fertilizers like rhizobacteria that promote
selected PGPR strains considerably reduces the impact of salt stress in plant growth. The use of PGPR strains to boost the yield of intercrops is a
wheat by activating the expression of tolerance genes (Gontia-Mishra promising tool in agricultural practice. Indeed, PGPR inoculants can be
et al., 2016). The PGPR ability of 1-aminocyclopropane-1-carboxylate defined as formulations containing one or more strains (or species) of
(ACC) deaminase activity is very important for enhancing drought beneficial bacteria (consortium), which can act synergistically by
stress tolerance in plants. Bacillus, Pseudomonas, and Enterobacter sp. mutually promoting their beneficial effects (Chhatre et al., 1996).

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I. Chamkhi et al. Industrial Crops & Products 183 (2022) 114958

Inoculation of plants with bacterial consortia often has a positive effect Indeed, they facilitate interspecific root interactions, requiring a mini­
on alleviating salt stress in plants. Using wheat as a test plant exposed to mum of N and P inputs, minimize competition for resources, use avail­
salt stress, to investigate the effects of selected bacterial consortia able resources efficiently, increase productivity mainly for non-legume
formulated using members of five genera: Enterobacter, Microbacterium, crops, and improve yield stability in stressful environments (Lith­
Serratia, Pseudomonas, and Achromobacter, demonstrated that inocula­ ourgidis et al., 2011). In addition, insurance against crop failure, soil
tion with selected halotolerant bacterial consortia significantly increases conservation, improvement of soil fertility, promotion of biodiversity,
the emergence, growth, biomass, and superoxide dismutase activity of improvement of forage quality (Sun et al., 2013), and reduction of pest
wheat seedlings exposed to salt stress. Therefore, it improves the po­ and disease incidence (Dwivedi et al., 2015) can be achieved with
tential of bacteria to reduce the salt stress effects on plants, especially intercropping. Indeed, the cultivation of legumes can be a major source
bacteria producing halotolerant indoleacetic acid (IAA) and 1-aminocy­ of biological nitrogen in the soil, through their ability to fix atmospheric
clopropane-1- carboxylate deaminase (ACCD) (Barra et al., 2016). N for plant use due to the symbiotic nature of the plant-rhizobium
On other hand, the ability of rhizobacteria to act as bioprotectors relationship, which represents a powerful option to reduce synthetic N
against oxidative stress is the most reasonable explanation for their fertilizers (Bedoussac et al., 2015). Biological agriculture is highly
beneficial effects on host plants. Including via induced systemic resis­ dependent on renewable resources and biological nutrient contribu­
tance has also been demonstrated under drought stress. However, tions. In the case of fixed N, it is achieved largely through the exploi­
inoculation with the rhizobacteria Pseudomonas aeruginosa, Bacillus tation of legume-rhizobia symbiosis or free nitrogen-fixing rhizobacteria
subtilis, and Trichoderma harzianum, alone or in a consortium, can pro­ that help to maintain and/or improve soil fertility by using N drawn
vide protection against the pathogen (Sclerotinia sclerotiorum). This from the atmosphere (Wani et al., 1995).
protection can be achieved through the increased defensive capacity However, intercropping cereals with grain legume crops facilitates
elicited by induced oxidative stress and increased tolerance by partially the improvement of soil N balance, because legume crops such as
increasing the H2O2 content and antioxidant enzyme activities (Jain cowpea, mungbean, soybean, and groundnuts are reported to from 80 to
et al., 2013). Furthermore, the application of a consortium of PGPR has a 350 kg N ha− 1 (Nyoki and Ndakidemi, 2016). As has been well docu­
better probability of improving the adaptability of plants exposed to mented in the literature, this agriculture practice is mainly related to the
stress conditions than the same bacteria used alone (Joshi et al., 2020). rhizosphere, the soil microbial diversity, particularly the bacterial
However, it is worth noting that the use of intercropping is a better community. This intercrops mainly concerned maize, wheat, soybean,
strategy to complement the role of inoculation. Consequently, the yield cowpea, and faba bean crops, and resulted in improved nitrogen bal­
increases in intercropping with rhizobial inoculation, have been linked ance, P availability, root exudates, increased microbial biomass, crop
to numerous factors such as efficient use of space, light, planting density, yield in dry season; illustrated by a network in Fig. 7 according to the
weather, water utilization efficiency, plant-bacteria interactions, and high-frequency of keywords. A network analysis was performed to
their direct and indirect actions on plants (Xu et al., 2008). Hence, identify trends in scientific research as reflected in the publications used
intercropping and intercropping-rhizobial inoculation influence the for the systematic review. The analysis using VoSviewer was performed
microbial abundance and community compositions in the rhizosphere on the text of titles and abstracts. Terms that did not contribute to the
such as total bacteria, total AOA, and AOB depending on the plant analysis were discarded. The larger the circle, the more frequently it
species and growth stage, as observed in maize or faba bean rhizosphere occurred. The shorter and/or thicker the line indicates high
(Zhang et al., 2015). In fact, the intercropping combined with rhizobial co-occurrence of interconnected terms. This threshold was reached by
inoculation exhibited stronger effects on AOB that consequently impact 237 terms out of a total number of 2266 terms counted in the reviewed
the nitrification in the rhizosphere (Zhang et al., 2015). publications. The top terms with the highest frequencies were “com­
Moreover, Sun et al. (2009) revealed that the intercropping and munity”, “rhizosphere”, “soil microbe”, “diversity index”, “bacteria
intercropping-rhizobial in the case of alfalfa-Siberian wild rye (Elymus quantity”, “acidobacteria”, “bacteroidota”, “soil enzyme activity”, “ni­
sibiricus) with rhizobia inoculation significantly impacts the microbial trogen”, “cropping systems”, “intercropping treatment”, “faba bean”,
biomass, the microbial activities (urease activity and invertase activity) “soybean” “maize”, “plant growth”, “dry season”, etc…(Fig. 7).
as well as the bacterial community composition (Nitrosomonas and Pursuant to this, intercropping legume system in combination with
Nitrosospira groups) in the rhizosphere. Furthermore, in the rhizosphere bacterial inoculation can achieve better yields through the imple­
of alfalfa, intercropping-rhizobial inoculation significantly increased mentation of beneficial plant-microbe interactions that will play a major
microbial biomass C compared to intercropping alone. Accordingly, the role against climate change effects and sustain agriculture.
rhizobacterial inoculation positively impacted soil enzymatic activities
(alkaline phosphatase and acid phosphatase activity) (Sun et al., 2013). 10. Conclusions and future prospects
Especially with nutrient amendment, intercropping and rhizobium
inoculation influence the performance of some leguminous and forage Abiotic stresses are devastating limiting factors for agriculture, and
cereal crops. Rhizobium inoculation, legume intercropping, and addi­ finding solutions to deal with them has always been a challenge in both
tion of P enhanced nodulation and increased nodule number and weight agricultural and natural ecosystems. The key elements to solving this
(Abusuwar and Omer, 2011). problem are to highlight appropriate farming practices such as inter­
cropping with legumes. 16–22% of the world’s food supply is still pro­
9. Intercropping with legume: perspectives for sustainable vided by multiple traditional cropping systems. It is important to note
agriculture in stress-affected areas that the legume species commonly used for the supply of grains and
green manures have the potential to fix between 100 and 300 kg N/ha− 1
Sustainable agriculture is increasingly encouraged for its benefits to from the atmosphere (the proportion of N derived from atmosphere
the environment and humanity. Intercropping systems adopt the prin­ fixation was about 40% in the intercropped soybean and 30% in the sole
ciple of sustainable agriculture which is based on the three pillars of crop without fertilizer application). In addition, the need for phosphate
sustainable development encompassing ecological, social, and economic fertilizer was 21% lower in intercrops compared to sole crops for the
aspects. This development is especially linked to the increased interest in same yields. This review reports that intercropping with legumes
low-input agriculture around the world to minimize environmental is­ significantly improves soil fertility, rhizobacteria community and di­
sues associated with the application of high agrochemical inputs, versity, and nutrient availability that are determinants of increased crop
including high N rates. The increased cultivation of legumes may offer growth performance. In this way, rhizobacteria have shown a great ca­
potential and important benefits. pacity to be explored for their various mechanisms of action to improve
Certainly, intercropping legume systems offer several advantages. the development and growth of plants under stress conditions. In the

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Fig. 7. Cluster density visualization map of 2266 terms, 237 meet the threshold and 142 no. of terms were selected (produced by VOSviewer 1.6.15).

rhizosphere, a successful bacteria-plant interaction can confer several Abusuwar, A., Omer, E., 2011. Effect of intercropping, phosphorus fertilization and
rhizobium inoculation on the growth and nodulation of some leguminous and cereal
properties such as growth stimulation, nutritional value, resistance to
forages. Int. J. Agric. Biol. 2, 109–124. https://doi.org/10.5251/
phytopathogens, and particularly the improvement of crop stress toler­ abjna.2011.2.1.109.124.
ance. These effects can be improved by the use of several rhizobacteria Adesoji, A., Abubakar, I., Labe, D., 2014. Soil chemical properties as affected by
with synergistic activities. In fact, the inoculation of plants with indi­ incorporated legumes and nitrogen in soil with maize (Zea mays L.) in a semi-arid
environment. Int J. Agric. Innov. Res. 3, 888–894.
vidual isolates or with bacterial consortia often has positive effects, in Alvey, S., Bagayoko, M., Neumann, G., Buerkert, A., 2001. Cereal/legume rotations affect
particular the alleviation of salt stress in plants. Moreover, it has long chemical properties and biological activities in two West African soils. Plant Soil
been noticed that these rhizobacteria mediated properties can be shared 231, 45–54. https://doi.org/10.1023/A:1010386800937.
Aly, AmalH., Debbab, A., Kjer, J., Proksch, P., 2010. Fungal endophytes from higher
between plants via a legume intercropping system. This mode of crop­ plants: a prolific source of phytochemicals and other bioactive natural products.
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in corn (Zea mays L.) and soybean (Glycine max L. Merrill) intercropping on soil
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nutrient availability, and acquisition of tolerance to abiotic stress, Armstrong, R.D., Kuskopf, B.J., Millar, G., Whitbread, A.M., Standley, J., 1999. Changes
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Declaration of Competing Interest increase in lower soil layers of water-limited faba bean intercropped with wheat.
J. Plant. Nutr. Soil Sci. 179, 537–546. https://doi.org/10.1002/jpln.201500533.
Bargaz, A., Noyce, G.L., Fulthorpe, R., Carlsson, G., Furze, J.R., Jensen, E.S., Dhiba, D.,
The authors declare that they have no known competing financial Isaac, M.E., 2017. Species interactions enhance root allocation, microbial diversity
interests or personal relationships that could have appeared to influence and P acquisition in intercropped wheat and soybean under P deficiency. Appl. Soil.
Ecol. 120, 179–188. https://doi.org/10.1016/j.apsoil.2017.08.011.
the work reported in this paper.
Barra, P.J., Inostroza, N.G., Acuña, J.J., Mora, M.L., Crowley, D.E., Jorquera, M.A., 2016.
Formulation of bacterial consortia from avocado (Persea americana Mill.) and their
Acknowledgement effect on growth, biomass and superoxide dismutase activity of wheat seedlings
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