JOURNAL OF PLANT PROTECTION RESEARCH

Vol. 56, No. 3 (2016)

DOI: 10.1515/jppr-2016-0043

Re v ie w

Management of soil-borne diseases of organic vegetables

Hafiza Asma Shafique1, Viqar Sultana2, Syed Ehteshamul-Haque1, Mohammad Athar3,4*

1 AgriculturalBiotechnology and Phytopathology Laboratory, Department of Botany, University of Karachi, Karachi 75270, Pakistan
2 Biotechnology and Drug Development Laboratory, Department of Biochemistry, University of Karachi, Karachi 75270, Pakistan
3 Post Harvest Technology and Food Biochemistry Laboratory, Department of Food Science and Technology, University of Karachi,

Karachi 75270, Pakistan

4 Present address: Pest Detection and Emergency Projects, California Department of Food and Agriculture,

3288 Meadowview Road, Sacramento, 95832 CA, USA

Received: March 10, 2016

Accepted: August 18, 2016

Abstract: With the rising awareness of the adverse effects of chemical pesticides, people are looking for organically grown vegetables.
Consumers are increasingly choosing organic foods due to the perception that they are healthier than those conventionally grown.
Vegetable crops are vulnerable to a range of pathogenic organisms that reduce yield by killing the plant or damaging the product,
thus making it unmarketable. Soil-borne diseases are among the major factors contributing to low yields of organic produce. Apart
from chemical pesticides there are several methods that can be used to protect crops from soil-borne pathogens. These include the
introduction of biocontrol agents against soil-borne plant pathogens, plants with therapeutic effects and organic soil amendments
that stimulate antagonistic activities of microorganisms to soil-borne diseases. The decomposition of organic matter in soil also results
in the accumulation of specific compounds that may be antifungal or nematicidal. With the growing interest in organic vegetables, it
is necessary to find non chemical means of plant disease control. This review describes the impact of soil-borne diseases on organic
vegetables and methods used for their control.

Key words: control, biological antagonists, organic manure, organic vegetables, seaweeds, soil-borne diseases

Introduction countries (of which about 15 are less developed) export

Rising awareness of the adverse effects of chemical pes- certified organic products, namely tropical and off-sea-
ticides and an increasing demand for organic fruits and son commodities (Willer and Yussefi 2004).
vegetables have encouraged growers to transit to sus- Soil biology is directly linked to agricultural sustain-
tainable and organic production systems (Klonsky 2004). ability as it is the driving force behind decomposition pro-
Such ecologically sound systems have the potential to cesses that break down complex organic molecules and
address a number of ongoing issues in mainstream ag- substances and convert them into plant available forms
riculture, namely pollution due to synthetic chemical (Friedel et al. 2001). Large, stable, and active soil microbial
fertilizers and pesticides, production losses due to pest communities are important for sustaining the productivi-
and disease pressure, soil degradation, loss of soil fertility ty of soils under sustainable and organic farming systems.
and productivity (Engindeniz and Cosar 2013). Organic To develop such systems growers adopt strategies such as
farming pursues a course of promoting self-regulation crop rotation, cover cropping, and application of organic
and resistance which plants and animals possess natu- amendments (manures and composts) that significantly
rally. Especially in poorer countries, it can contribute to increase soil organic matter (SOM) and improve soil biol-
purposeful socio-economic and ecologically sustain- ogy and quality (Buyer et al. 2010).
able development (Willer and Yussefi 2004). During the
last decade, many countries of the European Union, the The significance of organic vegetables
United States, and also countries in Latin America, Africa,
Asia and Oceania have experienced a significant increase According to the USDA (United States Department of
in certified organic farms. Almost 23 mln ha are managed Agriculture) National Organic Standards Board (NOSB),
organically worldwide. According to the International organic agriculture is defined as “an ecological produc-
Trade Center, annual sales grew from US $17.5 billion in tion management system that promotes and enhances
2000 to US $21 billion in 2001. Growth rates for 2003–2005 biodiversity, biological cycles, and soil biological activity.
are estimated to be from 5–15%. About 90 developing It is based on the minimal use of off-farm inputs and on

*Corresponding address:
[email protected]
222 Journal of Plant Protection Research 56 (3), 2016

management practices that restore, maintain or enhance and Xanthomonas groups usually persist in the soil for
ecological harmony. The primary goal of organic agricul- only a short time. Soil-borne viruses that infect vegetables
ture is to optimize the health and productivity of inter- are few in number and generally survive only in the liv-
dependent communities of soil life, plants, animals and ing tissues of the host plant or in insects, the nematode
people”. or fungal vectors that transmit them (Baysal-Gurel et al.
Consumers are becoming increasingly concerned 2012).
about how, where and when foods are produced. The de- Root-knot nematodes (Meloidogyne spp.) are seri-
mand for organic products is also increasing as people ous and economically the most important pest of many
become aware of the benefits of organic produce. This has cultivated crops around the world (Youssef and Lashein
led to an increased consumer interest in organically grown 2013). Root-knot nematodes are sedentary endoparasites
vegetables including those produced in greenhouses. One and are among the most damaging agricultural pests at-
of the core philosophies of organic production systems tacking a wide range of crops. They particularly damage
is the development of healthy and productive soil that vegetables in tropical and subtropical countries (Sikora
provides essential nutrients for plant growth, supports and Fernandez 2005; Adam et al. 2014) and cause losses
diverse and active soil biotic communities and balances of up to 80% in heavily infested fields. Economically root-
the entire farm ecosystem. There is a growing demand knot nematodes constitute the most important phyto-
for organic products since more and more consumers feel nematode. Collectively, they parasitize more than 2,000
that they are healthier than those conventionally grown plant species with vegetables and horticultural crops be-
(Yiridoe et al. 2007). Globally there are about 37,232,127 ha ing highly susceptible (Adam et al. 2014). Losses caused
of organically managed land with Australia accounting by plant parasitic nematodes are estimated to be about
for 32.2% (Paull 2011). It has been reported that overall US $100 billion annually (Saifullah et al. 2007).
organic produce contains 5.7% more micronutrients than Fusarium solani and R. solani are the most important
comparable conventionally grown produce (Hunter et al. soil-borne fungal pathogens, which develop in both cul-
2011). The annual global sale of organic food is estimated tured and non-cultured soils, causing damping-off and
to be about US $60 billion (Paull 2011). Organic food con- root rot diseases in a wide range of vegetable and crop
sumption is part of a way of life and is associated with plants including tomato (Szczechura et al. 2013). The inci-
a strong interest in nature, society and the environment dence of damping-off was increased from 19 to 90% with
(Schifferstein and Ophuis 1998). However, consumers are increasing inoculum levels of Rhizoctonia solani, while the
sometimes confused and the term ‘organic’ is interpreted incidence of root rots caused 10 to 80% losses in different
in a variety of ways. It is often associated with terms like vegetables. Rhizoctonia solani, an important destructive soil-
‘ecological’, ‘green’, ‘natural’ and ‘sustainable’ (Aarset et borne pathogen has detrimental effects on agricultural and
al. 2004). horticultural crops by pre-emergence and post-emergence
damping-off, root rot, and stem canker. Its host plants in-
Soil-borne diseases clude alfalfa, peanut, soybean, lima bean, cucumber, pa-
paya, eggplant, corn and many more (Keijer et al. 1997).
Soil-borne diseases are one of the major factors contrib- Macrophomina phaseolina, which causes charcoal rot,
uting to low yields of organic products. Vegetable crops is cosmopolitan in distribution and is a potential threat
are vulnerable to a range of pathogenic organisms that re- to crop production in arid regions (Ijaz et al. 2013). It is
duce yield by damaging whole plants or valued products a soil inhabiting fungus, an important root pathogen
and make them unmarketable. Plant diseases are respon- and causes dry root rot/stem canker, stalk rot or charcoal
sible for as much as 26% of yield loss in global agriculture rot in over 500 plant species (Khan 2007). The wide host
and sometimes there may be complete crop failure (Khan range of M. phaseolina suggests that it is a non-host-spe-
et al. 2009). Although the development of plant diseases cific fungus. Charcoal rot is of great economic importance
is a regular part of an ecosystem and crop production, in arid areas of the world and has been reported to be
it becomes a concern when the diseases assume an epi- the major limiting factor for sunflower production (Khan
demic form causing enormous crop losses (Morsy et al. 2007; Ijaz et al. 2013). Damping-off and root rot caused by
2009). Some of the most important soil-borne diseases the Pythium are considered to be among the most devas-
are caused by pathogens that are ‘soil inhabitants’, have tating diseases of greenhouse-grown crops. This patho-
broad host ranges that include weeds, and produce long- gen affects nearly every crop grown in every part of the
lived survival structures. Important soil-borne pathogens world. The main causal agent of the damping-off and
include fungi, fungi-like organisms, bacteria as well as root rot is Pythium aphanidermatum. Some Pythium species
viruses and plant parasitic nematodes (Baysal-Gurel et al. are among the most destructive plant pathogens (Agri-
2012). Fungal pathogens, including species of Fusarium, os 2005). The majority of Pythium species are capable of
Rhizoctonia, Verticillium, Sclerotinia and Macrophomina parasitizing seeds, seedlings, and older stages of a wide
phaseolina, cause the loss of billions of dollars each year. range of plants causing damping-off disease. However,
Many soil-borne fungi persist in the soil for long periods the greatest damage is done to the seeds and the roots of
by producing resistant survival structures such as chla- seedlings either before or after emergence (Agrios 2005).
mydospores, oospores and sclerotia (Baysal-Gurel et al. Phytophthora is a soil-borne fungus that can attack the
2012). Important soil-borne bacterial pathogens include roots, crown and fruits of many crop varieties (Fig. 1).
Ralstonia, Pectobacterium, Agrobacterium and Streptomyces The disease is more active under wet conditions and is
(Baysal-Gurel et al. 2012). Pathogens in the Pseudomonas spread by contamination of soil. Phytophthora capsici at-
 Soil-borne vegetable diseases 223

Fig. 1. Okra field infected with Fusarium and Phytophthora

tacks a wide variety of vegetables, fruits, grains and floral cover cropping, application of organic amendments (ma-
crops. It may remain viable for 10 years or more in soil nures and composts) and biological antagonists (Shafique
(Baysal-Gurel et al. 2012). It is difficult to estimate yield et al. 2015a, b). Along with cover crops, the use of compost
losses due to Phytophthora diseases since the same species and manure is considered to be an integral component
may cause a number of other diseases, in different envi- of organic production since it provides essential plant
ronmental conditions, particularly rainfall and humidity, nutrients and improves soil quality and structure (Russo
can have a dramatic effect on disease incidence and sever- and Webber 2007). The elucidation of the effect of such al-
ity (Benson et al. 2006). Most Phytophthora-related losses ternative practices on soil-borne pathogens is needed for
can be attributed to Phytophthora pod rot (PPR) followed the design of soil and crop management systems that are
by stem cankers. It is commonly estimated that 10–20% of also suppressive to soil-borne pathogens and their root
the world’s annual production is lost due to PPR, but esti- diseases. Several books and review articles have been
mates vary from average annual losses of 10% up to 30%, published on this subject including ways to assess and
with much higher losses in particularly wet locations or quantify it (Doran et al. 1994).
during wet years (Erwin and Ribeiro 2006). In Western
Samoa, losses of 60–80% due to PPR in wet years were Plant products
reported by Keane (1992).
Plants with therapeutic effects have received the atten-
Control of soil-borne diseases tion of scientists as an alternate method of disease control
which protects the environment from the use of hazard-
Most soil-borne pathogens are difficult to control by con- ous chemicals. Crop rotation, in general, provides numer-
ventional strategies such as the use of resistant cultivars ous benefits to crop production. Application of botanical
and synthetic pesticides (Weller et al. 2002). Soil applica- toxicants or plant products has been reported to reduce
tion of fungicides is expensive and deleterious to non- root-knot disease (Al-Askar 2012; Khalil et al. 2012). They
target microflora. Biological control has become a critical can help conserve, maintain, or replenish soil resources,
component of plant disease management and it is a prac- including organic matter, nitrogen and other nutrient in-
tical and safe approach in various crops (Patel and Ana- puts, as well as physical and chemical properties (Ball et
hosur 2001). Bioprotectants provide a unique opportunity al. 2005; Ladygina and Hedlund 2010). Crop rotation has
for crop protection, since they grow, proliferate, colonize been associated with increased soil fertility, increased soil
and protect the newly-formed plant parts to which they tilth and aggregate stability, improved soil water manage-
were not initially applied. Soil biology is directly linked ment and reduced erosion (Ball et al. 2005). For example,
to agricultural sustainability since it is the driving force crops in the Brassicaceae family which include broccoli,
behind decomposition processes that break down com- cabbage, cauliflower, turnip, radish, canola, rapeseed and
plex organic molecules and substances and convert them various mustards, produce sulfur compounds that break
into plant available forms (Friedel et al. 2001). A large, sta- down to produce isothiocyanates that are toxic to many
ble and active soil microbial community is an underpin- soil organisms as part of a process referred to as biofumi-
ning for maintaining the productivity of soils under sus- gation (Youssef and Lashein 2013). Use of these plants as
tainable and organic farming systems. To develop such rotation, cover, or green manure crops has been observed
systems growers adopt such strategies as crop rotation, to reduce soil-borne diseases or populations of fungal
224 Journal of Plant Protection Research 56 (3), 2016

pathogens and nematodes and to improve soil characteris- Compost when properly prepared and used can help
tics and crop yield (Larkin and Griffin 2007). Further stud- and promote low-input agricultural systems to become
ies have indicated that additional mechanisms, including more sustainable and productive (Golabi et al. 2003). Ma-
specific changes in soil microbial communities unrelated tured composts, even without microbial inoculation, are
to levels of toxic metabolites, are also important in the re- already valuable. However, continuing research shows
duction of soil-borne diseases by Brassica crops (Mazzola that options which employ microbial inoculation in com-
et al. 2004; Larkin and Griffin 2007). Crop rotation is one of post tend to further improve its productivity. Composted
the most effective tools for managing pests and maintain- manure thus has a more long-term role in building soil
ing soil fertility. A common approach on vegetable farms is fertility, and has been shown to be more effective in build-
to rotate crops by families. Another strategy is to alternate ing soil microbial biomass and increasing activity than
vegetable crops with field or forage crops such as small uncomposted manure (Fließach and Mäder 2000). Simi-
grains, alfalfa or clovers. Some growers try to rotate fields larly, additions of large quantities of organic matter were
so they are in cash crops one year and cover crops the next found to create anaerobic conditions that contributed to
year. Sweet corn is a good crop to rotate with since it hosts the reduction of inoculums of Fusarium oxysporum f. sp.
very few insects or diseases that affect other vegetables. asparagi, R. solani and V. dahliae (Blok et al. 2000).
For diseases that are soil-borne or over-winter in crop resi- Compost extract contains a high population of mi-
dues, rotating out of susceptible crops is a key in prevent- crobiota, e.g. rhizobacteria, Trichoderma and Pseudomo-
ing infection, as in the case of Phytophthora blight, early nas spp., which may enhance growth and yield of crops
blight, and many other diseases. (Welke 2005). These microbiota produce plant growth
It is known that plants and plant products (organic hormones and chemical compounds (e.g. siderophores,
amendments, crop residues, green manures) can dramati- tannins, phenols) which are antagonistic to various soil
cally affect soil microbial communities, and are primary pathogens. The use of compost extract is also claimed
drivers of soil microbial dynamics (Hoitink and Boehm to increase soil C levels, improve soil structure, nutri-
1999; Garbeva et al. 2004), and thus may be important com- ent cycling and water holding capacity, and suppress
ponents in establishing and maintaining soil suppressive- plant diseases (Ghorbani et al. 2008). However, to achieve
ness. Crop rotations and residue amendments have been these benefits, several variables have to be considered to
shown to have major effects on soil microbial communi- produce compost extracts of the desired quality. These
ties and can result in significant reductions in soil-borne include microbial food sources, compost to water ratio,
diseases (Abawi and Widmer 2000; Bailey and Lazarovits levels of aeration, compost quality, compost age, dura-
2003). Green manures of cabbage and cauliflower leaves, tion of incubation, and the quality of water used. There is
chopped pineapple leaves, dry straw of rice, rye or oats also a need for consistent compost quality which depends
and cotton wastes are reported to reduce the incidence of on consistency of inputs and methods used to produce
root-knot in the field (Youssef and Lashain 2013). compost. Organic matter amendments to soil have been
shown to have beneficial effects on soil nutrients, physi-
Organic manures cal condition and biological activity as well as crop viabil-
ity (Hulugalle et al. 1986).
With the rising popularity of organic farming due to ad- Besides a wide variety of organic matters that have
verse effects of chemicals, the organic fertilizer industry been tested as organic amendments for managing plant
is growing rapidly (Sultana et al. 2011b). Organic amend- pathogens, oil seed cakes decreased the population of
ments are generally used for improving crops, increas- soil-borne pathogens (Shafique et al. 2015b). Oil seed
ing agricultural productivity and suppressing soil-borne cakes are by-products obtained after oil extraction from
diseases (Hoitink and Boehm 1999; Stone et al. 2003). The seeds. Oil seed cakes are of two types, edible and non-
quantity of nutrients in manures varies with the type of edible. Non-edible oil seed cakes such as castor cake and
animal, feed composition, quality and quantity of bed- neem cake are used as organic nitrogenous fertilizers,
ding material, length of storage and storage conditions due to their NPK content. Some of these oil cakes have
(Dewes and Hunsche 1998). The application of organic been found to increase the nitrogen uptake by the plant
amendments has been proposed as a strategy for the and protect the plants from soil nematodes, insects, and
management of diseases caused by soil-borne pathogens. parasites (Ramachandran et al. 2007). Several antimicrobi-
Organic amendments with organic wastes, composts and al by-products (e.g. organic acids, hydrogen sulfide, phe-
peats, have been proposed to control diseases caused by nols, tannins and nitrogenous compounds) are released
soil-borne pathogens. There are many examples of soil- during the decomposition of organic amendments, or
borne pathogens controlled effectively by the application synthesized by microorganisms involved in such degra-
of organic amendments: like Gaeumannomyces graminis dation (Rodríguez-Kábana et al. 1995).
f. sp. tritici, M. phaseolina, R. solani, Thielaviopsis basicola,
Verticillium dahliae, species of Fusarium, Phytophthora, Py- Seaweed fertilizers
thium and Sclerotium (Bonanomi et al. 2007). Tuitert et al.
(1998) reported that un-decomposed and mature com- Application of seaweeds as an organic soil amendment
posts were suppressive to R. solani damping-off, but par- has increased in recent years due to rising awareness of
tially decomposed materials were conducive. Compost the adverse effects of chemical pesticides (Mazzola 2004;
extracts are gaining popularity particularly among those Sultana et al. 2011b). The high fiber content of seaweed
who are seeking substitutes to agrochemicals (Bess 2000). acts as a soil conditioner and assists moisture retention,
 Soil-borne vegetable diseases 225

while the mineral content is a useful fertilizer and source Several antagonistic organisms have been success-
of trace elements (Mat-Atko 1992). They also contain bio- fully used as biocontrol agents for controlling soil-borne
control properties and contain many organic compounds pathogens (Afzal et al. 2013; Kowsari et al. 2014). In most
and growth regulators such as auxins, gibberellins and of the research to date, biocontrol agents are applied sin-
precursor of ethylene and betaine which affect plant gly to combat the growth of pathogens. Although the
growth. Seaweed extracts have been reported to increase potential benefits of a single biocontrol agent application
plant resistance to pests and diseases, plant growth, yield has been demonstrated in many studies, but in many
and quality (Mat-Atko 1992). Seaweeds contain elaborate, cases they showed inconsistent performance because
secondary metabolites that play a significant role in the a single biocontrol agent is not likely to be active in all
defense of the host against pathogens and parasites (Ara kinds of soil environments and all agricultural ecosys-
et al. 2005). Seaweed could affect cell metabolism through tems (Raupach and Kloepper 1998). These have resulted
the induction of the synthesis of antioxidant molecules in inadequate colonization, limited tolerance to changes
which could favor plant growth and plant resistance to in environmental conditions and fluctuations in the pro-
stress (Zhang and Schmidt 2000). Anti-oxidant enzymes duction of antifungal metabolites (Weller et al. 2002).
provide a degree of crop protection from free radical Mixtures of biocontrol agents also have the advantage of
oxidants arising from normal metabolism and any num- exercising a broad spectrum activity, in general enhanc-
ber of biotic and abiotic stresses. Wu et al. (1997) dem- ing the efficacy and reliability of biological control and
onstrated that the betaines present in different extracts ensuring greater induction of defense enzymes over in-
decreased nematode infestation. Furthermore, seaweeds dividual strains (Latha et al. 2009). A highly effective bio-
suppressed root rotting fungi and the root-knot nema- control strain should be able to both compete and persist
tode by producing antimicrobial compounds or synthesis in the environment and to colonize and proliferate on
of antioxidant molecules. Seaweeds contain 1-aminocy- plant parts. It should be very inexpensive and maintain
clopropane-1-carboxylic acid (ACC), which has antimi- good viability without a specialized storage system (Har-
crobial activity (Nelson and van Standen 1985). Similarly, man 1996).
polyphenols are well known for their antioxidant activity Soil application of biocontrol agents viz. Trichoderma
and are widely distributed in seaweeds (Tariq et al. 2011). viride, T. harzianum, fluorescent Pseudomonas and Bacil-
A red seaweed Solieria robusta used as a soil amendment lus subtilis effectively reduced root rot caused by soil-
showed better suppression of root rotting fungus F. so- borne pathogens in several crops (Loganathan et al. 2010;
lani than Topsin-M (Sultana et al. 2011a). Soil amendment Shafique et al. 2015b). Trichoderma spp. are known to
with seaweed was also found to be effective in reduc- produce large quantities of fungi toxic metabolites. The
ing root-knot infection besides improving plant growth inhibitory effect of Trichoderma spp. might be due to di-
both in field plots and farmers’ fields (Baloch et al. 2013). rect mycoparasitism in addition to competition for nu-
Seaweeds were also found effective on eggplant, a plant trients (Sharon et al. 2001; Afzal et al. 2013). Trichoderma
which is highly susceptible to root-knot nematode under spp. are active mycoparasites that have been considered
field conditions (Baloch et al. 2013). Liquid concentrations for biocontrol of foliar and soil-borne diseases as well as
of brown algae Ecklonia maxima significantly reduced plant parasitic soil-borne nematodes (Kowsari et al. 2014).
root-knot infestation and increased the growth of tomato Trichoderma spp. can provide excellent control against
plants. It has also been shown that seaweeds occurring root-knot nematodes such as T. harzianum (Sharon et al.
on the Karachi, Pakistan coast have nematicidal, fungi- 2001), and are viewed as strong contenders for develop-
cidal and antibacterial properties (Ara et al. 2005) and soil ment as biocontrol agents. However, differences in the
amendment with seaweeds with or without a biocon- efficacy among isolates, their biocontrol potential and
trol agent significantly reduced the root-knot nematode the reproducibility of results under different conditions
(Meloidogyne javanica) and root infecting fungi on various have impeded their development (Sharon et al. 2001).
crops (Sultana et al. 2011a, b). Increasingly, Trichoderma spp. are being investigated for
their biocontrol potential against root-knot nematodes on
Biological antagonists a range of crops, such as tomato, okra, mungbean and bell
pepper (Meyer et al. 2001). Afzal et al. (2013) found that
With the rising awareness of the adverse effects of chemi- endophytic T. viride was effective in suppressing the F. so-
cal pesticides interest in the introduction of biocontrol lani, F. oxysporum and root-knot nematode on okra used
microbes into the rhizosphere is increasing. Different alone or with Pseudomonas aeruginosa (Fig. 2).
mechanisms of biocontrol agents are supposed to con- Chaetomium, Penicillium and Trichoderma species are
tribute to the suppression of soil-borne plant pathogens, biological control agents that have the potential to control
parasitism, production of antifungal compounds, com- plant diseases. Naraghi et al. (2010) reported successful
petition for nutrients and colonization sites, and induc- biological control of tomato verticillium disease by an-
tion of systemic resistance in plants against pathogens. tagonistic effects of Talaromyces flavus. Field trials have
Disease suppressive composts containing biological con- shown that Chaetomium formulated bioproducts have
trol agents are the major component of the total product. promise as broad spectrum mycofungicides to control
Van Bruggen (1995) found that cellulolytic and hemi- many diseases (Soytong et al. 2001). Similarly the appli-
cellulolytic actinomycetes were present in much higher cation of bioproducts from Chaetomium can protect and
numbers in organically amended soils than those using cure Thielaviopsis bud rot of Hyophorbe lagenicaulis in Thai-
chemical fertilizers. land (Soytong et al. 2001). It is well known that actinomy-
226 Journal of Plant Protection Research 56 (3), 2016

Fig. 2. Effect of endophytic Trichoderma viride (TV) and Pseudomonas aeruginosa (PA) on infection of Fusarium solani (dark bar) and
F. oxysporum (white bar) on okra roots

cetes produce 70–80% of bioactive secondary metabolites, sarium crown and root rot and Phytophthora disease on
where approximately 60% of antibiotics developed for tomato (Cordier 1996) and Verticillium wilt of cotton (Liu
agricultural use are isolated from Streptomyces spp. (Ilic 1995). Enhanced nutrient status of the plant for VAM cit-
et al. 2007). It has an enormous biosynthetic potential that rus, high arginine levels in VAM tobacco that were inhibi-
remains unchallenged, and is without a potential compet- tory to pathogen chlamydospores and cell thickenings
itor among other microbial groups (Solanki et al. 2008). in VAM onion which restricted pathogen penetration
Many reports have pointed out that since streptomyce- (Pfleger and Linderman 2000) were found.
tes are frequently screened for antimicrobial activity, the The plant growth promoting rhizobacteria (PGPR)
existence of secondary metabolites with other activities are rhizospheric microbes which produce bioactive sub-
may have been missed (Garcia et al. 2000). This microbi- stances and promote plant growth and/or protect them
al wealth from actinomycetes has yet to be investigated against pathogens. Root colonizing bacteria that have
thoroughly. Similarly inoculation of soil with Paecilomyces a beneficial effect on plants are termed plant growth pro-
lilacinus resulted in considerable reduction of nematode moting rhizobacteria and are reported to improve plant
multiplication. The ability of P. lilacinus to control nema- growth either through direct stimulation of the plant by
todes increased when it was integrated with organic mat- producing growth regulators or by suppression of patho-
ters. It is assumed that the decomposition of organic mat- gens (Raaijmakers et al. 2002). Of the various rhizospheric
ter released nematicidal properties and residual organic bacteria, the bacteria belonging to the fluorescent Pseudo-
matter increased fungal activity and persistence (Mani monas which colonize roots of a wide range of crop plants
and Anandam 1989). A combined use of P. lilacinus with are reported to be antagonistic to soil-borne plant patho-
P. aeruginosa has been found to be more effective in re- gens (Siddiqui and Ehteshamul-Haque 2001). The pro-
ducing the infection of root-infecting fungi and root-knot duction of certain antibiotics (Raaijmakers et al. 2002) and
nematode on pumpkin, guar, chili and watermelon (Per- siderophores (De Meyer and Hofte 1997) by P. aeruginosa
veen et al. 1998). Paecilomyces lilacinus, besides parasitiz- has been regarded as one of the mechanisms involved in
ing eggs of root-knot and cyst nematodes also produced antagonism. Raajimakers and Weller (1998) reported the
nematicidal metabolites (Jatala et al. 1990). role of 2,4-diacetylphloroglucinol, an antifungal metabo-
In addition to antagonistic fungi and bacteria the ar- lite from species of fluorescent Pseudomonas in plant root
buscular mycorrhizal fungi (AMF) have also been used disease suppression.
against soil-borne diseases (Berta et al. 2005). Vesicular
arbuscular endo-mycorrhizas, the most common type of Induction of systemic resistance by PGPR and antagonistic
mycorrhizal association, are formed by nearly all cultivat- fungi against diseases, insect and nematode pests
ed plants whether they are agricultural, horticultural or
fruit crops (Pfleger and Linderman 2000). The importance Several possible mechanisms including the production
of this type of symbiotic fungal infection for plant min- of antifungal metabolites, competition for space and nu-
eral nutrition and more generally for plant health (Sood trients, mycoparasitism, plant growth promotion and in-
2003), makes it potentially one of the more useful biologi- duction of the defense responses in plants have been sug-
cal means of assuring plant production with a minimum gested as mechanisms for their biocontrol activity (How-
input of chemicals such as fertilizers or pesticides (Pfleger ell 2003). When identifying potential biocontrol agents,
and Linderman 2000). Vesicular arbuscular mycorrhizae antifungal metabolites produced by them are important
(VAM) enhance plant growth through increased nutrient factors to be taken into account. Many research groups
uptake, stress tolerance and disease resistance (Bouamri are actively trying to find metabolites produced by bio-
et al. 2006). There are reports that VAM decrease the se- control agents which will suppress particular diseases
verity of disease caused by plant pathogenic fungi (Filion (Dowling and O’Gara 1994). Certain biochemical changes
et al. 2003). Vesicular arbuscular mycorrhizae can reduce occurring after the application of biocontrol agents can
damage from Rhizoctonia on several plant species and act as markers for induced systemic resistance. These in-
other plant pathogen combinations (Berta et al. 2005), Fu- clude accumulation of certain enzymes, such as peroxi-
 Soil-borne vegetable diseases 227

dase (Govindappa et al. 2010). Among the new biological management approach or practice such as a biological
approaches, the stimulation of natural plant defenses is amendment or crop rotation, alone will probably not be
considered to be one of the most promising alternative effective in establishing disease suppression, but multi-
strategies for crop protection (Walters and Fountaine ple approaches such as combinations of rotations, cover
2009). This original biological approach does not exert crops, organic and biological amendments, need to be op-
direct effects on the pathogen (Walters and Fountaine timized and coordinated together as part of an integrated
2009) but stimulates natural defenses in plants, leading to soil management program. Active management of soil
a systemic acquired resistance (Goel and Paul 2015). The microbial communities for disease suppression through
induction of plant defense mechanisms was associated the use of effective crop rotations and biological amend-
with the production of elicitors by the plant-host (endog- ments has much potential, but more research is needed
enous elicitor) (Montesano et al. 2003). The accumulation to determine the effects and interactions among microor-
of salicylic acid (SA) during systemic acquired resistance ganisms, the most effective crop and amendment combi-
is preceded by a transient increase in phenylalanine am- nations and their practical implementation.
monia-lyase (PAL) activity and inhibition of PAL activity
suppresses the systemic acquired resistance (Mandal et al.
Acknowledgements
2009). The systemic activation of the defense mechanisms
was accompanied by a systemic acquired resistance to in- We are thankful to Dr. David Goorahoo, California State
sects, nematodes, fungi, bacteria and viruses (Bakker et al. University, Fresno, CA, Dr. Surendra Dara, University of
2013). Salicylic acid is now the focus of intensive research California Cooperative Extension, San Luis Obispo, CA,
due to its function as an endogenous signal mediating lo- Prof. Dr. Riaz Ahmad, Oklahoma State University, Still-
cal and systemic plant defense responses against patho- water, OK, USA, Prof. Dr. Daniel Sanchez-Mata, Univer-
gens. It has also been found that SA plays a role during sity of Complutense, Madrid, Spain, Dr. Moazzam Niza-
the plant response to abiotic stresses such as drought, mi, Chinese Academy of Sciences, Yunnan, China and Dr.
chilling, heavy metal toxicity, heat, and osmotic stress. Viliana Vasileva, Forage Crop Institute, Pleven, Bulgaria
In this sense, SA appears to be an ‘effective therapeutic for their comments, criticism and suggestions during
agent’ for plants. The discovery of its targets and the un- preparation of this manuscript.
derstanding of its molecular modes of action in physi-
ological processes could help in the dissection of the com-
plex SA signaling network (Vicente and Plasencia 2011).
References
Aarset B., Beckmann S., Bigne E., Beveridge M., Bjorndal T., Bun-
ting J., McDonagh P., Mariojouls C., Muir J., Prothero A.,
Conclusion Reisch L., Smith A., Tveteras R., Young J. 2004. The Europe-
Organic farming is gaining worldwide acceptance and is an consumers’ understanding and perceptions of the ‘‘or-
becoming a major tool for sustaining the quality of de- ganic” food regime: The case of aquaculture. British Food
graded soils due to the intensive use of synthetic chemi- Journal 106 (2): 93–105.
cals for increasing crop production. The use of bio-agents, Abawi G.S., Widmer T.L. 2000. Impact of soil health management
such as biofertilizers or biopesticides is an integral part practices on soilborne pathogens, nematodes and root dis-
of organic farming especially in vegetable cultivation. eases of vegetable crops. Applied Soil Ecology 15 (1): 37–47.
The nature of the organic amendments, the microor- Adam M., Heuer H., Hallmann J. 2014. Bacterial antagonists of
ganisms present, the properties of the soil, and environ- fungal pathogens also control root-knot nematodes by in-
mental conditions are key factors that can influence the duced systemic resistance of tomato plants. PLoS ONE 9
populations of soil-borne plant pathogens and the crop (2): e90402. DOI: 10.1371/journal.pone.0090402
to be protected. Using organic amendments, antagonistic Afzal S., Tariq S., Sultana V., Ara J., Ehteshamul-Haque S. 2013.
microorganisms and phytochemicals in controlling soil- Managing the root diseases of okra with endo-root plant
borne root infecting fungi offers an alternate strategy to growth promoting Pseudomonas and Trichoderma viride as-
the prevalent use of synthetic pesticides. Mixtures of bio- sociated with healthy okra roots. Pakistan Journal of Bota-
control agents have the advantage of exercising a broad ny 45 (4):1455–1460.
spectrum activity, enhancing the efficacy and reliability of Agrios G.N. 2005. Plant Pathology. Academic Press, New York,
biological control and ensuring greater induction of de- USA, 952 pp.
fense enzymes in an individual. However, in many cases Al-Askar A.A.A. 2012. In vitro antifungal activity of three Saudi
the application of more than one biocontrol agent did not plants extracts against some phytopathogenic fungi. Jour-
yield any added advantage. nal of Plant Protection Research 52 (4): 458–462.
Plant growth in organic systems greatly depends on Ara J., Sultana V., Qasim R., Ehteshamul-Haque S., Ahmad V.U.
the functions performed by soil microbes particularly in 2005. Biological activity of Spatoglossum asperum: a brown
nutrient supply. The build-up of a large and active soil alga. Phytotherapy Research 19 (7): 618–623.
microbial biomass, therefore, is critically important for Bailey K.L., Lazarovits G. 2003. Suppressing soil-borne diseases
sustaining the productivity of soils in organic farming with residue management and organic amendments. Soil
systems. More research is needed to identify and char- and Tillage Research 72 (2): 169–180.
acterize locally available amendments and the impact of Bakker P.A.H.M., Doornbos R.F., Zamioudis C., Berendsen R.L.,
antagonistic organisms as related to potential soil-borne Pieterse C.M.J. 2013. Induced systemic resistance and the
pathogen control. This review also indicated that a single
228 Journal of Plant Protection Research 56 (3), 2016

rhizosphere microbiome. The Plant Pathology Journal 29 Engindeniz S., Cosar G.O. 2013. An economic comparison on
(2): 136–143. pesticide applications for processing and table tomatoes:
Ball B.C., Bingham I., Rees R.M., Watson C.A., Litterick A. 2005. a case study for Turkey. Journal of Plant Protection Re-
The role of crop rotations in determining soil structure and search 53 (3): 230–237.
crop growth conditions. Canadian Journal of Soil Science Erwin D.C., Ribeiro O.K. 1996. Phytophthora Diseases World-
85 (5): 557–577 wide. The American Phytopathological Society Press, St.
Baloch G.N., Tariq S., Ehteshamul-Haque S., Athar M., Sultana Paul, MN, USA, 562 pp.
V., Ara J. 2013. Management of root diseases of eggplant Filion M., St-Arnaud M., Jabaji-Hare S.H. 2003. Quantification
and watermelon with the application of asafoetida and of Fusarium solani f. sp. phaseoli in mycorrhizal bean plants
seaweeds. Journal of Applied Botany and Food Quality 86: and surrounding mycorrhizosphere soil using real-time
138–142. polymerase chain reaction and direct isolations on selec-
Baysal-Gurel F., Gardener B.M., Miller S.A. 2012. Soilborne tive media. Phytopathology 93 (2): 229–235.
disease management in organic vegetable production. Fließach A., Mäder P. 2000. Microbial biomass and size-density
Available on: www.extension.org/pages/64951. [Accessed: fractions differ between soils of organic and conventional
February 28, 2016] agricultural systems. Soil Biology and Biochemistry 32 (6):
Benson D.M., Grand L.F., Vernia C.S., Gottwald T.R. 2006. Tem- 757–768.
poral and spatial epidemiology of Phytophthora root rot in Friedel J.K., Gabel D., Stahr K. 2001. Nitrogen pools and turnover
Fraser fir plantations. Plant Disease 90 (9): 1171–1180. in arable soils under different durations of organic farm-
Berta G., Sampo S., Gamalero E., Massa N., Lemanceau P. 2005. ing. II: Source- and-sink function of the soil microbial bio-
Suppression of Rhizoctonia root-rot of tomato by Glomus mass or competition with growing plants? Journal of Plant
mossae BEG12 and Pseudomonas fluorescens A6RI is associ- Nutrition and Soil Science 164 (4): 421–429.
ated with their effect on the pathogen growth and on the Garbeva P., van Veen J.A., van Elsas J.D. 2004. Microbial diversity
root morphogenesis. European Journal of Plant Pathology in soil: selection of microbial populations by plant and soil
111 (3): 270–288. type and implications for disease suppressiveness. Annual
Bess V.H. 2000. Understanding compost tea. BioCycle 41 (10): Review of Phytopathology 42: 243–270.
71–72. Garcia I., Job D., Matringe M. 2000. Inhibition of p-hydroxyphe-
Blok W.J., Lamers J.G., Termorshuizen A.J., Bollen G.J. 2000. Con- nylpyruvate dioxygenase by the diketonitrile of isoxa-
trol of soilborne plant pathogens by incorporating fresh or- flutole: a case of half-site reactivity. Biochemistry 39 (25):
ganic amendments followed by tarping. Phytopathology 7501–7507.
90 (3): 253–259. Ghorbani R., Koocheki A., Jahan M., Asadi G.A. 2008. Impact of
Bonanomi G., Antignani V., Pane C., Scala F. 2007. Suppression of organic amendments and compost extracts on tomato pro-
soilborne fungal diseases with organic amendments. Jour- duction and storability in agroecological systems. Agrono-
nal of Plant Pathology 89 (3): 311–324. my for Sustainable Development 28 (2): 307–311.
Bouamri R., Dalpé Y., Serrhini M.N., Bennani A. 2006. Arbuscu- Goel N., Paul P.K. 2015. Polyphenol oxidase and lysozyme medi-
lar mycorrhizal fungi species associated with rhizosphere ate induction of systemic resistance in tomato, when a bioe-
of Phoenix dactylifera L. in Morocco. African Journal of Bio- licitor is used. Journal of Plant Protection Research 55 (4):
technology 5 (6): 510–516. 343–350.
Buyer J.S., Teasdale J.R., Roberts D.P., Zasada I.A., Maul J.E. 2010. Golabi M.H., Marler T.E., Smith E., Cruz F., Lawrence J.H., Den-
Factors affecting soil microbial community structure in to- ney M.J. 2003. Use of compost as an alternative to synthetic
mato cropping system. Soil Biology and Biochemistry 42 fertilizers for crop production and agricultural sustainabil-
(5): 831–841. ity for the island of Guam. Food and Fertilizer Technology
Cordier C., Gianinazzi S., Gianinazzi-Pearson V. 1996. Coloniza- Center, Taipei, Taiwan, R.O.C. Available on: http://www.
tion patterns of root tissues by Phytophthora nicotianae var. fftc.agnet.org/library.php?func=view&id=20110808092915.
parasitica related to reduced disease in mycorrhizal tomato. [Accessed: February 17, 2016]
Plant and Soil 185 (2): 223–232. Govindappa M., Lokesh S., Ravishankar Rai V., Rudra Naik V.,
De Meyer G., Höfte M. 1997. Salicylic acid produced by rhizobac- Raju S.G. 2010. Induction of systemic resistance and man-
terium Pseudomonas aeruginosa 7NSK2 induced resistance agement of safflower Macrophomina phaseolina root-rot dis-
to leaf infection by Botrytis cinerea on bean. Phytopathology ease by biocontrol agents. Archives of Phytopathology and
87 (6): 588–593. Plant Protection 43 (1): 26–40.
Dewes T., Hünsche E. 1998. Composition and microbial degrad- Harman G.E. 1996. Trichoderma for biocontrol of plant pathogens:
ability in the soil of farmyard manure from ecologically- from basic research to commercialized products. In: Pro-
managed farms. Biological Agriculture and Horticulture 16 ceedings of the Cornell Community Conference on Biologi-
(3): 251–268. cal Control, Ithaca, NY, 11–13 April 1996.
Doran J.W., Coleman D.C., Bezdicek D.F., Stewart B.A. 1994. De- Hoitink H.A.J., Boehm M.J. 1999. Biocontrol within the context
fining Soil Quality for a Sustainable Environment. Soil Sci- of soil microbial communities: a substrate-dependent phe-
ence Society of America, Special Publications Number 35, nomenon. Annual Review of Phytopathology 37: 427–446.
Madison, WI, USA, 244 pp. Howell C.R. 2003. Mechanisms employed by Trichoderma species
Dowling D.N., O’Gara F. 1994. Metabolites of Pseudomonas in- in the biological control of plant diseases: the history and
volved in the biocontrol of plant disease. Trends in Biotech- evolution of current concepts. Plant Disease 87 (1): 4–10.
nology 12 (4): 133–141. Hulugalle N.R., Lal R., Ter Kuile C.H.H. 1986. Amelioration of
soil physical properties by Mucuna after mechanized land
 Soil-borne vegetable diseases 229

clearing of a tropical rain forest. Soil Science 141 (3): 219– Loganathan M., Sible G.V., Maruthasalam S., Saravanakumar
224. D., Raguchander T., Sivakumar M., Samiyappan R. 2010.
Hunter D., Foster M., McArthur J.O., Ojha R., Petocz P., Sam- Trichoderma and chitin mixture based bioformulation for
man S. 2011. Evaluation of the micronutrient composition the management of head rot (Sclerotinia sclerotiorum (Lib.)
of plant foods produced by organic and conventional ag- de Bary) – root-knot (Meloidogyne incognita Kofoid and
ricultural methods. Critical Reviews in Food Science and White; Chitwood) complex diseases of cabbage. Archives
Nutrition 51 (6): 571–582. of Phytopathology and Plant Protection 43 (10): 1011–1024.
Ijaz S., Sadaqat H.A., Khan M.N. 2013. A review of the impact Mandal S., Mallick N., Mitra A. 2009. Salicylic acid-induced re-
of charcoal rot (Macrophomina phaseolina) on sunflower. The sistance to Fusarium oxysporum f. sp. lycopersici in tomato.
Journal of Agricultural Science 151 (2): 222–227. Plant Physiology and Biochemistry 47 (7): 642–649.
Ilic S.B., Konstantinovic S.S., Todorovic Z.B., Lazic M.L., Veljkov- Mani A., Anandam R.J. 1989. Evolution of plant leveas, oil cakes
ic V.B., Jokovic N., Radovanovic B.C. 2007. Characteriza- and agro-industrial wastes as substrates for mass multipli-
tion and antimicrobial activity of the bioactive metabolites cation of the nematophagus fungus, Paecillomyces lilacinus.
in streptomycete isolates. Microbiology 76 (4): 421–428. Journal of Biological Control 3 (3): 56–58.
Jatala P., Manrique G., Gavilano L. 1990. Nematicidal efficiency of Mat-Atko J. 1992. Experiments with the preparation Bio-Algeen
some fungal metabolites and their specificity in controlling S-90 in hops. Chemelarstvi 65: 53.
plant parasitic nematodes. Fitopatología 25 (1): 13. Mazzola M. 2004. Assessment and management of soil microbial
Keane P.J. 1992. Diseases of pests and cocoa: an overview. p. community structure for disease suppression. Annual Re-
1–11. In: “Cocoa Pest and Disease Management in South- view of Phytopathology 42 (1): 35–59.
east Asia and Australasia” (P.J. Keane, C.A.J. Putter, eds.). Meyer S.L.F., Roberts D.P., Chitwood D.J., Carta L.K., Lums-
Food and Agriculture Organization of the United Nations, den R.D., Mao W. 2001. Application of Burkholderia cepacia
Rome, Italy, 223 pp. and Trichoderma virens, alone and in combinations, against
Keijer J., Korsman M.G., Dullemans A.M., Houterman P.M., De Meloidogyne incognita on bell pepper. Nematropica 31 (1):
Bree J., Van Silfhout C.H. 1997. In vitro analysis of host 75–86.
plant specificity in Rhizoctonia solani. Plant Pathology 46 Montesano M., Brader G., Palva E.T. 2003. Pathogen derived
(5): 659–669. elicitors: searching for receptors in plants. Molecular Plant
Khalil M.E.H., Allam A., Barakat A.T. 2012. Nematicidal activity Pathology 4 (1): 73–79.
of some biopesticides and microorganisms against root- Morsy E.M., Abdel-Kawi K.A., Khalil M.N.A. 2009. Efficiency of
knot nematode on tomato plants under greenhouse con- Trichoderma viride and Bacillus subtilis as biocontrol agents
ditions. Journal of Plant Protection Research 52 (1): 47–52. against Fusarium solani on tomato plants. Egyptian Journal
Khan M.R., Altaf S., Mohiddin F.A., Khan U., Anwer A. 2009. of Phytopathology 37 (1): 47–57.
Biological control of plant nematodes with phosphate Naraghi L., Heydari A., Rezaee S., Razavi M., Jahanifar H.,
solubilizing microorganisms. p. 395–426. In: “Phosphate Khaledi E.M. 2010. Biological control of tomato Verticil-
Solubilizing Microbes for Crop Improvement” (M.S. Khan, lium wilt disease by Talaromyces flavus. Journal of Plant
A. Zaidi, eds.). Nova Science Publishers, New York, NY, Protection Research 50 (3): 360–365.
USA, 451 pp. Nelson W.R., Van Staden J. 1985. 1-Aminocyclopropane-1-car-
Khan S.N. 2007. Macrophomina phaseolina as causal agent or char- boxylic acid in seaweed concentrate. Botanica Marina 28
coal rot of sunflower. Mycopathology 5 (2): 111–118. (9): 415–417.
Klonsky K. 2004. Organic agricultural production in California. Patel S.T., Anahosur K.H. 2001. Potential antagonism of Tricho-
p. 241–256. In: “California Agriculture: Dimensions and derma harzianum against Fusarium spp. and Macrophomina
Issues” (J. Siebert, ed.). University of California, Giannini phaseolina and Sclerotium rolfsii. Journal of Mycology and
Foundation of Agricultural Economics, Division of Agri- Plant Pathology 31: 365–366.
culture and Natural Resources, Berkeley, CA, USA, 304 pp. Paull J. 2011. Organics Olympiad 2011: Global indices of leader-
Kowsari M., Motallebi M., Zamani R.M. 2014. Construction of ship in organic agriculture. Journal of Social and Develop-
new GFP-tagged fusants for Trichoderma harzianum with ment Sciences 1 (4): 144–150.
enhanced biocontrol activity. Journal of Plant Protection Perveen S., Ehteshamul-Haque S., Ghaffar A. 1998. Efficacy of
Research 54 (2): 122–131. Pseudomonas aeruginosa and Paecilomyces lilacinus in the
Ladygina N., Hedlund K. 2010. Plant species influence microbial control of root rot-root knot disease complex of some veg-
diversity and carbon allocation in the rhizosphere. Soil Bio- etables. Nematologia Mediterranea 26 (2): 209–212.
logy and Biochemistry 42 (2): 162–168. Pfleger F.L., Linderman R.G. 2000. Mycorrhiza and Plant
Larkin R.P., Griffin T.S. 2007. Control of soilborne potato dis- Growth. The American Phytopathological Society Press,
eases using Brassica green manures. Crop Protection 26 (7): St. Paul, MN, USA, 360 pp.
1067–1077. Raaijimakers J.M., Vlami M., de Souza J.T. 2002. Antibiotic pro-
Latha P., Anand T., Ragupathi N., Prakasam V., Samiyappan R. duction by bacterial biocontrol agents. Antonie van Leeu-
2009. Antimicrobial activity of plant extracts and induc- wenkoek 81 (1–4): 537–547.
tion of systemic resistance in tomato plants by mixtures Raaijimakers J.M., Weller D.M. 1998. Natural plant protection by
of PGPR strains and Zimmu leaf extract against Alternaria 2,4-diacetylphloroglucinol producing Pseudomonas spp. in
solani. Biological Control 50 (2): 85–93. take-all decline soils. Molecular Plant-Microbe Interactions
Liu R.J. 1995. Effect of vesicular-arbuscular mycorrhizal fungi on 11 (2): 144–152.
Verticillium wilt of cotton. Mycorrhiza 5 (4): 293–297.
230 Journal of Plant Protection Research 56 (3), 2016

Ramachandran S., Singh S.K., Larroche C., Soccol C.R., Pandey diseases in field-grown snap bean and cucumber. Plant
A. 2007. Oil cakes and their biotechnological applications – Disease 87 (9): 1037–1042.
A review. Bioresource Technology 98 (10): 2000–2009. Sultana V., Baloch G.N., Ambreen, Ara J., Tariq M.R., Ehtesham-
Raupach G.S., Kloepper J.W. 1998. Mixtures of plant growth pro- ul-Haque S. 2011a. Comparative efficacy of a red alga
moting rhizobacteria enhance biological control of multiple Solieria robusta, chemical fertilizers and pesticides in man-
cucumber pathogens. Phytopathology 88 (11): 1158–1164. aging the root diseases and growth of soybean. Pakistan
Rodríguez-Kábana R., Estaún V., Pinochet J., Marfá O. 1995. Mix- Journal of Botany 43 (1): 1–6.
tures of olive pomace with different nitrogen sources for Sultana V., Baloch G.N., Ara J., Ehteshamul-Haque S., Tariq
the control of Meloidogyne spp. on tomato. Supplement to R.M., Athar M. 2011b. Seaweeds as an alternative to chemi-
the Journal of Nematology 27 (4S): 575–584. cal pesticides for the management of root diseases of sun-
Russo V.M., Webber III C.L. 2007. Organic agricultural produc- flower and tomato. Journal of Applied Botany and Food
tion in the United States: an old wheel being reinvented. Quality 84 (2): 162–168.
The Americas Journal of Plant Science and Biotechnology Szczechura W., Staniaszek M., Habdas H. 2013. Fusarium oxyspo-
1 (1): 29–35. rum f. sp. radicis-lycopersici – the cause of Fusarium crown
Saifullah M., Stephen M., Khattak B. 2007. Isolation of Tricho- and root rot in tomato cultivation. Journal of Plant Protec-
derma harzianum and in vitro screening for its effectiveness tion Research 53 (2): 172–178.
against root-knot nematodes (Meloidogyne sp.) from Swat, Tariq A., Ara J., Sultana V., Ehteshamul-Haque S., Athar M. 2011.
Pakistan. Pakistan Journal of Nematology 25 (2): 313–322. Antioxidant potential of seaweeds occurring at Karachi
Schifferstein H.N.J., Ophuis P.A.M. 1998. Health-related deter- coast of Pakistan. Journal of Applied Botany and Food
minants of organic food consumption in the Netherlands. Quality 84 (2): 207–212.
Food Quality and Preference 9 (3): 119–133. Tuitert G., Szczech M., Bollen G.J. 1998. Suppression of Rhizoc-
Shafique H.A., Noreen R., Sultana V., Ara J., Ehteshamul-Haque tonia solani in potting mixtures amended with compost
S. 2015a. Effect of endophytic Pseudomonas aeruginosa and made from organic household waste. Phytopathology 88
Trichoderma harzianum on soil-borne diseases, mycorrhizae (8): 764–773.
and induction of systemic resistance in okra grown in soil van Bruggen A.H.C. 1995. Plant disease severity in high-input
amended with Vernonia anthelmintica (L.) seed’s powder. compared to reduced-input and organic farming systems.
Pakistan Journal of Botany 47 (6): 2421–2426. Plant Disease 79 (10): 976–984.
Shafique H.A., Sultana V., Ara J., Ehteshamul-Haque S., Athar Vicente M.R., Plasencia J. 2011. Salicylic acid beyond defense: its
M. 2015b. Role of antagonistic microorganisms and organ- role in plant growth and development. Journal of Experi-
ic amendment in stimulating the defense system of okra mental Botany 62 (10): 3321–3338.
against root rotting fungi. Polish Journal of Microbiology Walters D.R., Fountaine J.M. 2009. Practical application of in-
64 (2): 157–162. duced resistance to plant diseases: an appraisal of effec-
Sharon E., Bar-Eyal M., Chet I., Herrera-Estrella A., Kleifeld O., tiveness under field conditions. The Journal of Agricultural
Spiegel Y. 2001. Biological control of the root-knot nema- Science 147 (05): 523–535.
tode Meloidogyne javanica by Trichoderma harzianum. Phyto- Welke S.E. 2005. The effect of compost extract on the yield of
pathology 91 (7): 687–693. strawberries and the severity of Botrytis cinerea. Journal of
Siddiqui I.A., Ehteshamul-Haque S. 2001. Suppression of the Sustainable Agriculture 25 (1): 57–68.
root rot-root knot disease complex by Pseudomonas aerugi- Weller D.M., Raaijimakers J.M., Gardener B.B.M., Thomashow
nosa in tomato: The influence of inoculum density, nema- L.S. 2002. Microbial populations responsible for specific
tode populations, moisture and other plant associated bac- soil suppressiveness to plant pathogens. Annual Review of
teria. Plant and Soil 237 (1): 81–89. Phytopathology 40: 309–348.
Sikora R.A., Fernández E. 2005. Nematode parasites of veg- Willer H., Yussefi M. 2004. The World of Organic Agriculture – Sta-
etables. p. 319–392. In: “Plant Parasitic Nematodes in Sub- tistics and Emerging Trends 2004. International Federation
tropical and Tropical Agriculture.” 2nd ed. (M. Luc, R.A. of Organic Agriculture Movements, Bonn, Germany, 167 pp.
Sikora, J. Bridge, eds.). CABI Publishing, Willingford, Ox- Wu Y., Jenkins T., Blunden G., Whapham C., Hankins S.D. 1997.
fordshire, UK, 896 pp. The role of betains in alkaline extracts of Ascophyllum nodo-
Solanki R., Khanna M., Lal R. 2008. Bioactive compounds from sum in reduction of Meloidogyne javanica and M. incognita
marine actinomycetes. Indian Journal of Microbiology 48 infestations of tomato plants. Fundamental and Applied
(4): 410–431. Nematology 20 (2): 99–102.
Sood S.G. 2003. Chemotactic response of plant growth-promot- Yiridoe E.K., Bonti-Ankomah S., Martin R.C. 2007. Comparison
ing bacteria towards roots of vesicular-arbiscular mycor- of consumer perceptions and preference toward organic
rhizal tomato plants. FEMS Microbiology Ecology 45 (3): versus conventionally produced foods: A review and up-
219–227. date of the literature. Renewable Agriculture and Food
Soytong K., Kanokmadhakul S., Kukongviriyapa V., Isobe M. Systems 20 (04): 193–205.
2001. Application of Chaetomium species (Ketomium®) as Youssef M.M.A., Lashein A.M.S. 2013. Effect of cabbage (Bras-
a new broad spectrum biological fungicide for plant dis- sica oleracea) leaf residue as a biofumigant, on root knot
ease control: A review article. Fungal Diversity 7: 1–15. nematode, Meloidogyne incognita infecting tomato. Journal
Stone A.G., Vallad G.E., Cooperband L.R., Rotenberg D., Darby of Plant Protection Research 53 (3): 271–274.
H.M., James R.V., Stevenson W.R., Goodman R.M. 2003. Zhang X., Schmidt R.E. 2000. Hormone-containing products’ im-
The effect of organic amendments on soilborne and foliar pact on antioxidant status of tall fescue and creeping bent-
grass subjected to drought. Crop Science 40 (5): 1344–1349.