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Biological control of plant nematodes with phosphate solubilizing

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Chapter 19

BIOLOGICAL CONTROL OF PLANT NEMATODES WITH PHOSPHATE- SOLUBILIZING

MICROORGANISMS

Mujeebur Rahman Khan1, Shahana Altaf2, Fayaz A Mohidin3,

Uzma Khan4 and Arshad Anwer5
1,4,5
Department of Plant Protection, Faculty of Agricultural Sciences, Aligarh Muslim University
Aligarh 202 002, India; 2UCSF Medical Cancer, University of California, San Francisco, USA;
3
Department of Botany, University of Kashmir, Srinagar, India

Correspondence to: mrkhan777in@yahoo.co.in

ABSTRACT
Plant nematodes are important pests of agricultural crops and cause singnificant crop damage
throughout the world. Management of nematode may be achieved by applying phosphate-solubilizing
microorganisms. Experiments conducted mostly under pot conditions have revealed that soil application
or seed treatment with the fungi such as, Aspergillus niger, Penicillium digitatum, P. anatolicum,
Paecilomyces lilacinus, Trichoderma spp. etc. reduced the crop damage, reproduction and soil
population of some important ecto- and endop-parasitic nematodes. Culture filtrates of these fungi
inhibited the hatching of eggs and induced mortality to nematode larvae in vitro. The use of
phosphate-solubilizing bacteria in nematode management has been extensively employed, and the
results have demonstrated that application of effecient strains of Bacillus subtilis, B. polymyxa,
Pseudomonas fluorescens, P. stutzeri, P. striata etc. effectively controlled the nematodes and
profoundly improved the crop yields. Overall performance of phosphate-solubilizing microorganisms
against plant nematodes have been found to a level that ensures their commercial exploitation. This
necessitates further in-depth studies under field condition in different agro-climates. Development of
efficient immobilizing systems which could support the longer survival of the PSMs and also their
multiplication during storage and marketing is likely to prove critical in commercializing such microbes
in crop protection.

1
 19.1. INTRODUCTION
Plant parasitic nematodes are considered important pathogens of agricultural crops. Nematodes
cause damage to plants by injuring and feeding on the root hairs, epidermal cells, cortical and/or stealer
cells [Khan, 2008]. A large number of nematodes, like, Tylenchus, Hoplolaimus, Rotylenchus,
Helicotylenchus, Tylenchorhynchus, Belonolaimus, Trichodorus and Longidorus are ectoparasites
feeding on root surface. However, a considerable number of nematodes enter fully inside the host root
and are called endoparasites, such as, root-knot nematodes [Meloidogyne spp.], cyst forming nematodes
[Heterodera spp.] and root-lesion nematode [Pratylenchus spp.]. Whereas some nematodes such as,
citrus nematode [Tylenchulus semipenetrans] and reniform nematode [Rotylenchulus reniformis] are
semi-endoparasites as they partially enter the host tissue. The most common effect of nematode
parasitism is debilitation of the plant with a symptom of stunting of plant growth and mild yellowing of
foliage that resembles with nutritional deficiency. As a result, instead of namaticide, fertilizer is applied
by farmers which prove ineffective and noneconomic.
Nonspecific or general symptoms of nematode infestation appear as patches of plants irregularly
distributed in a field showing stunted growth, sparse and dull green or pale yellow foliage [Luc et al.,
2005]. The infested plants show incipient wilting despite adequate soil moisture during sunny days but
recover at night. Further, roots so weakened and damaged by nematodes are easily invaded by many
bacteria and fungi, leading to accelerated root decay. This secondary damage also does not draw
immediate attention and an incurable stage is soon reached leading to severe yield losses [Khan and
Reddy, 1993] both quantitatively and qualitatively under subtropical and tropical conditions [Sasser,
1989]. For example, Molya of wheat [Heterodera avenae], ufra of rice [Ditylenchus angustus], root rot
of maize [Pratylenchus zeae], root-knot of cereals, pulses [Meloidogyne spp.] etc. are some of the
diseases which cause tremendous economic loss to all kind of crops [Luc et al., 2005]. Nematodes may
cause about 7-12% yield loss to various crops. The yield losses vary greatly depending on inoculum
level and host species. The severe infection may result to as much as 80-90% yield decline in an
individual field and sometimes plants fail to give yield of economic value. However, nematodes do not
always cause hidden damage. When fields are heavily infested, characteristic symptoms appear on roots
or shoots. Specific symptoms include root-lesions, root-rot, root pruning, root-galls, cessation of root
growth etc. [Khan, 2008] [Fig. 1]. Some nematodes also cause characteristic symptoms on above ground
parts. For example, Anguina tritici causes seed galls and as a result, normal grains of wheat, barley and
oat turn brown to black and irregular in shape. Similarly leaf tips of rice become white due to infection
of Aphelenchoides besseyi. In addition to direct damage, nematodes often aid or aggravate the diseases
caused by fungi, bacteria and viruses or may break resistance of cultivars to pathogens. Hairy root of
2
 A B
A

C D

Fig. 1 Symptoms of nematode infection in plants, root necrosis caused by Pratylenchus sp. [A] root galls
by Meloidogyne spp. [B] cysts by Globodera sp. [C] and seed galls by Anguina tritici [D].

roses caused by Agrobacterium rhizogenes is of minor importance, but in the presence of Pratylenchus
vulnus the disease becomes severe [Sitaramaiah and Pathak, 1993]. The fusarium wilt resistant cultivars
of cotton become susceptible in the presence of root-knot nematodes [Atkinson, 1892]. The crop
damage, however, depends largely on the plant species or cultivar, nematode species, level of soil
infestation and the prevailing environmental conditions. Plant nematodes may also act as vector for
bacteria, fungi and viruses. For instance, Anguina tritici carries Clavibacter tritici and Dilophospora
alopecuri to shoot meristem of wheat [Khan and Dasgupta, 1993]. Nematode transmitted polyhedral
viruses [NEPO], which are ringspot viruses for example, tobacco ring spot virus, is transmitted by
Xiphinema and Longidorus species. Trichodorus and Paratrichodorus species act as vector for certain
tobra viruses such as tobacco rattle and pea early browning viruses [Taylor and Brown, 1997].

3
 Despite a significant impact on agriculture, nematodes have not been recognized as major pest of
crops, probably because of the damage caused by nematodes is less obvious than that caused by fungi or
other pathogens. Crop losses due to nematodes are greater in the developing countries than the
developed countries. It is probably due to unplanned agricultural practices, unawareness of the farmers
about nematodes and non availability of nematicides. In the developed countries where management
practices are properly implemented, the nematode damages are relatively low; still causing
considerable yield losses. Foe example annual monetary loss due to nematodes has been estimated over
$ 6.0 billion in USA alone [Agrios, 2005].
In the high input agricultural practices, the control of pests and pathogens using biological
preparation seems quite difficult due to wide application of chemical pesticides. However, there are
numerous instances where one or the other antagonistic organism has reduced the populations of plant
pathogens including plant nematodes. For example, suppression of cereal-cyst nematode, Heterodera
avenae found in certain soils [suppressive] under monocultures of susceptible cereals in northern Europe
is the best example of natural control of any plant-parasitic nematode [Kerry, 1982]. The suppression is
attributed to the population build up of parasitic fungi Pochonia chlamydosporia [Verticillium
chlamydosporium] as continuous monoculturing leads to parasitization of the developing females
resulting in 95-97% reduction in nematode population [Kerry et al., 1982].There are also some other
microorganisms that have demonstrated considerable potential antagonism against plant nematodes
[Stirling, 1993; Khan, 2005].
Biological control of nematodes may be achieved with two kinds of microorganisms. Classical
parasites or predators (e.g., Paecilimyces lilacinus, Dactylaria candida, Pasteuria penetrans) have been
used in the nematode control since old times (Khan and Khan, 1995). In recent years, interest has also
been developed in using plant growth promoting microorganisms. Of these, phosphate-solubilizing
microorganisms [PSM] are most important and may prove efficient biocontrol agents of plant
nematodes. The PSMs may suppress rhizosheric nematode populations by promoting host growth,
inducing systemic resistance and/or producing nematoxic metabolites [Kirkpatric et al., 1964], like,
bulbiformin [Brannen, 1995], phenazin [Toohey, 1965] and pyoleutorin [Howell and Stepinovic, 1980].
Nematode management employing phosphate-solubilizing fungi or bacteria has advantage over classical
biocontrol agents as the former provide essential nutrients to plants in addition to their nematode
inhibiting ability. Aspergillus niger, Penicillium spp., Trichoderma, Bacillus subtilis, B. polymyxa,
Pseudomonas fluorescens, P. stutzeri, P. striata, nematophagous fungus Arthrobotrys oligospora etc.
are some of the promising phosphate-solubilizers inhabiting agricultural soils [Gaur, 1990, Rao, 1990;
Rudresh et al., 2005; Duponnois et al., 2006; Pandy et al., 2008] and possess promising potential of
4
nematode antagonism. In the following section, the role of these fungi and bacteria in nematode
management is discussed.

19.2. PHOSPHATE-SOLUBILIZING FUNGI IN NEMATODE MANAGEMENT

Numerous phosphate-solubilizing fungi in addition to providing essential nutrients [Thomas et
al. 2005] including solubilizing insoluble P [Turan 2006] and consequently making it available to plants
[Mittal et al., 2008], are also known to suppress plant nematodes [Table 1] [Khan et al., 2000;
Oyekanmi, et al., 2008]. Phosphate-solubilizing fungi may directly affect the various developmental
stages of nematodes viz., eggs, larvae and adults [Pocasangre et al., 2007, Pant and Pandey, 2001;
Oyekanmi, et al., 2008; Sharon et al., 2009]. The phosphate-solubilizing fungi may suppress plant
parasitic nematodes through the following mechanisms of action.
19.2.1 Antibiosis
Antibiosis is the phenomenon of suppression of one organism by the other due to release of some
toxic substances/metabolites in the environment. Antibiosis provides a competitive saprophytic
advantage to phosphate-solubilizing fungi including species of Trichoderma, Aspergillus and
Penicillium [Lipping et al., 2008]. Low molecular weight compounds or antibiotics [both volatile and
non volatile] produced by Trichoderma species and Aspergillus spp. impede colonization of harmful
microorganisms including nematodes in the root zone [Eapen and Venugopal 1995]. Harzianic acid,
alamethicins, tricholin, peptaibols, antibiotics, 6-penthyl-α-pyrone, massoilactone, viridin, gliovirin,
glisoprenins, heptelidic acid, oxalic acid and enzymes are some of the chemicals produced by
Trichoderma and Aspergillus species [Mankau, 1969, a, b; Benitez et al. 2004; El-Hasan et al., 2007].
19.2.2 Stimulation of host defense response
The ability of phosphate-slubilizing fungi including strains of Trichoderma, Aspergillus niger,
and Penicillium digitatum to protect plants against root pathogens has long been attributed to its
antagonistic effect against the invading pathogen [Chet et al., 1997; Vassilev et al., 2006]. Strains of
Trichoderma may induce hypersensitive response [HR], systemic acquired resistance [SAR] and
induced systemic resistance [ISR] in plants [Harman et al., 2004]. Enzymes such as, phenyl alanine
ammonia lyase [PAL] and chalcone synthase [CHS] are produced that trigger the biosynthesis of
phytoalexins, chitinases and glucanases which may oppose nematode feeding. Trichoderma spp. may
induce host resistance by producing metabolites which may act as elicitors of plant resistance. Such
metabolites may also induce expression of genes responsible for synthesis of phytoalexins, PR proteins
or other compounds involved in increasing resistance against plant pathogens. It has been reported that

5
T. harzianum induced resistance in bean [Meyer et al., 1998], cucumber [Koike et al., 2001] and cotton
[Hanson and Howell, 2004].

Table 1. Effect of different phosphate solubilizing fungi on plant parasitic nematode infesting
agricultural crops.
Phosphate solubilizing fungi Nematode managed Host plant Reference
Aspergillus niger Meloidogyne Tomato Singh et al. [1991]
incognita
A. niger M. incognita Okra Sharma et al., [2005]
A. niger M. incognita Tomato Khan and Anwer [ 2007]
Paecilomyces lilacinus Root-knot nematode, - Pal and Gardener [2006]
Meloidogyne spp.
P. lilacinus Meloidogyne spp. Tomato Schenek [2004]
P. lilacinus Meloidogyne Tobacco Hewelett et al., [1988]
javanica
P. lilacinus R. reniformis Ttomato Lysek [1966]
P. lilacinus Meloidogyne species Numerous Jatala [1986]
crops
P. lilacinus Meloidogyne species Okra. Khan and Ejaz [1997]
Penicillium anatoticum Globodera Potato Jatala [1986]
rostochinensis
T. harzianum, P. lilacinus M. incognita Chickpea Pant and Pandey [2002]
T. harzianum and P. fluorescens M. javanica Tomato Siddiqui and Shaukat
[2004]
T. harzianum M. arenaria, Corn Windham et al [1989]
T. harzianum Meloidogyne spp. Cardamom IISR [1995]
Trichoderma asperellum-203 and M. javanica - Sharon et al. [2009]
Trichoderma atroviride
T. pseudokoningii, T. viride, P. M. incognita Soybean Oyekanmi et al. [2008]
lilacinus, A.niger, G.mosseae ,
P. fluorescens and P. putida
T. harzianum, P. lilacinus Meloidogyne Okra Zareen et al. [2001]
javanica
T. atroviride R. similis Banana Felde et al., [2006]
Pocasangre et al., [2007]
T. harzianum [T014] and M. incognita Gladiolus Khan and Mustafa [2005]
Pseudomonas fluorescens [PS
07]
P. chlamydosporia and T. Globodera Potato Saifullah [1996a, b]
harzianum rostochiensis and G.
pallid
T. harzianum and P. H. cajani Pigeonpea. Siddiqui and Mahmood
chlamydosporia [1996]

19.2.3 Plant growth promotion by phosphate-solubilizing fungi

6
 Root colonization by phosphate-solubilizing fungi frequently enhance root growth and
development, crop productivity, resistance to abiotic stresses and the uptake and use of nutrients
[Mehmet et al., 2005; Shin et al., 2006; Morales et al., 2007; Wakelin et al., 2007]. Crop productivity in
fields can increase up to 300% after the addition of T. hamatum or T. koningii or A. niger. The
experiments carried out in green houses with seed treatment with Trichoderma spores have shown
significantly greater yield [Chet et al., 1997]. Equal degree of yield enhancement was observed when
plant seeds were separated from Trichoderma by a cellophane membrane. This indicates that
Trichoderma produces growth factors that enhanced the rate of seed germination, plant growth and yield
[Benitez et al., 1998]. Trichoderma strains and A. niger that produce cytokinin like molecules, e.g.
zeatyn and gibberellin GA3 or GA3 have been recently detected. The controlled production of these
compounds could improve biofertilization. Thus, the plant growth promotion may be due to production
of plant hormones or increased uptake of nutrients by the plant [Chet et al., 1993]; control of one or
more sub potential pathogens [Baker, 1986] and/or strengthening plant’s own defense mechanism
[Zimand et al., 1996]. The most important genera of phosphate-solubilizing fungi and their mode of
action against plant pathogenic fungi or nematode is discussed in detail in the following paragraphs.
19.2.3.1 Aspergillus niger van Teigh in nematode management
Systematic position

Division Ascomycota
Sub division Pezizomycotina
Class Eurotiomycetes
Order Eurotiales
Family Trichocomaceae
Genus Aspergillus

Aspergillus niger is a versatile and abundant microorganism present in almost all soil types and
climates. The fungus is an important group of phosphate-solubilizer [Varenyam et al., 2007] and
possesses great potential to antagonize plant nematodes. Several studies have been conducted to
ascertain the biocontrol potential of A. niger against plant parasitic nematodes [Goswami et al., 1994;
Walia, 1994; Khan and Tarannum, 1999; Khan and Kounsar, 2000; Hasan, 2004; Khan et al., 2006].
Sharma et al. [2005] evaluated the effect of joint application of Kalisena [a commercial formulation of
A. niger AN 27 SD] and T. harzianum as seed treatment [1% w/w] on okra cv. Pusa Kranti against M.
incognita alone and in combination with carbofuran applied @0.5 kg/ha. The combined treatments with
Kalisena and T. harzianum and carbofuran were more effective and reduced root-knot galling by 20-
25% in comparison to sole application. Comparatively, T. harzianum was better than the Kalisena in
reducing the root-knot damage in combined application but plant growth was better in sole treatment of
7
bioagents than the combined application of carbofuran. Mittal et al. [2005] reported that degree of
antagonism by A. niger against plant parasitic nematodes vary with the strain/isolate of the fungus. Khan
et.al. [2006] collected 20 isolates of A. niger from different crops and locations and examined their
effectiveness against M. incognita in vitro and in vivo conditions. Three isolates were found more
aggressive and produced ammonia, hydrogen cyanide, siderophores and solubilised P in vitro. Culture
filtrates of these isolates greatly suppressed the hatching and mortality of M. incognita. A pot trial
conducted to test the effects on the root-knot disease on eggplant showed significant decrease in the gall
formation and egg mass production especially by A. niger isolates AnC2, AnR3 and AnM3 [Khan et al.,
2006]. Khan and Anwer [2007] also reported that different isolates of A. niger aggregates suppressed the
galling, egg mass production and decreased the soil population of M. incognita.
Effect of A. niger on the fungus nematode disease complex of pulses and vegetables has been
examined by researchers. Singh et.al. [1991] conducted a pot experiment to study the effect of M.
incognita alone and in combination with A. niger and R. solani on tomato cv. Perfection. Damage was
greatest in plants inoculated with M. incognita and R. solani together followed by the fungus and
nematode alone respectively. Damage to the plant was less when A. niger was inoculated with the
nematode. In another investigation Rekha and Sexena [1999] reported that A. niger, E. purphurascum
and P. vermiculatum effectively diluted the adverse effect of both the pathogens and showed an increase
in germination when incorporated in soil together with M. incognita or R. solani either separately or in
combination. During the last couple of years some field trials have been conducted to control disease
complexes. For instance, Haseeb and Kumar [2005] studied efficacy of A. niger, P. lilacinus, T.
harzianum, T. virens and P. fluorescens on M. incognita and F. solani disease complex of brinjal and
found all the treatments effectively reduced fungus infection and root galls. Anwer and Khan [2005]
isolated 40 isolates of A. niger from different crops and localities and evaluated thier effectiveness
against root-knot – root rot [M. incognita-R. solani] disease complex of eggplant cv Pusa Kranti and
found that application of A. niger isolates checked the galling and reproduction of nematode, decreased
the root rot index and improved the growth variables. Among various isolates, isolate AnC2 was found
highly effective.
19.2.3.2 Penicillium Thoms. in nematode management
Systematic position

Division Ascomycota
Sub division Pezizomycotina
Class Eurotiomycetes
Order Eurotiales
Family Trichocomaceae
8
 Genus Penicillium
Researchers through out the world have recognized the role of Penicillium spp. in the
biologically mediated soil nutrition. Commonly occurring Penicillium spp. in agricultural soils are P.
digitatum, P. lilaciumum, P. anatolicum etc. [Lal, 2002].Workers in India and abroad have also found
nematode suppressing effects of Penicillium spp. Inoculation with Penicillium anatolicum reduced the
Globodera rostochinensis population in Panama without parasitizing the female nematodes [Jatala
1986]. It appears to produce a series of compounds that can alter the permeability of the eggshell to
cause free movement of noxious compounds, which it has produced or were present in the soil, into the
eggs. This in turn may alter the egg physiology when it occurs in early stages of embryonic
development, causing abortive embryonic development and complete vacuolation of eggs within a short
period of time. Exposure of G. pallida cysts to these compounds from certain culture filtrates caused
reduction in hatching of the eggs due to the effects mentioned above [Jatala et al., 1985; O’Hara 1985].
Apparently when these compounds are liberated in the vicinity of the developing females of G.
rostochinensis and G. pallida, they cause deformation of females, which become evident as the females
mature to form cysts [Jatala 1986].
19.2.3.3 Trichoderma Persoon in nematode management
Systematic position

Division Amastigomycota
Sub division Deuteromycotina
Class Hyphomycetes
Order Moniliales
Family Moniliaceae
Sub family Gliosporae
Genus Trichoderma
Besides being a potent antifungal agent Trichoderma has also been used as an effective tool in
nematode management and have shown a variable degree of parasitism and mode of action [Pocasangre
et al., 2007, Pant and Pandey, 2001; Oyekanmi, et al., 2008; Sharon et al., 2009]. Paecilomyces lilacinus
is an obligate parasite of root-knot and other nematodes [Pal, 2006]. Eapen and Venugopal [1995]
reported that isolates of Trichoderma species have antagonistic potential against a variety of fungi and
nematodes. A serine protease gene [28 kDa] with trypsin activity was isolated from Trichoderma strain
2413. The enzyme reduced the number of hatched eggs of root knot nematodes and acted synergistically
with other proteins. Strains of Trichoderma species and bacteria Burkholderia cepacia are known to
produce extracellular compounds that inhibit egg hatching and motility of M. incognita juveniles [J2].
The number of hatched eggs of the root knot nematode, Meloidogyne incognita was significantly
reduced after incubation with pure PRA1 [trypsin like protease] preparations T. harzianum CECT 2413
9
[Suarez et al., 2004]. Pant et al. [2002] studied the effect of using T. harzianum and neem cake alone
and in combination to manage M. incognita in chickpea cv. Type-3. Greatest reduction in the root knot
nematode was recorded with the application of neem cake and T. harzianum together, followed by neem
cake and T. harzianum alone.
The green house studies reveals that, individual application of these microbes as seed treatment
followed by root drenching considerably suppress root-knot nematode on bell pepper compared with
untreated plants [Meyer et al., 2001]. Pant and Pandey [2001] recorded highest degree of suppression in
M. incognita population by T. harzianum, P. lilacinus and A. niger applied @ 5000 spores/pot.
Significant reduction in M. incognita was also observed when T. harziaum was applied along with the
neem cake [Pant and Pandey, 2002]. Siddiqui and Shaukat [2004] reported that combined application of
T. harzianum and P. fluorescens in unsterilized soil [sandy loam] caused greatly reduced population
densities of M. javanica in tomato. T. harzianum when applied before corn seeding in pots having M.
arenaria infested soil there was increase in fresh weight [shoot and root] with a decrease in the number
of eggs per gram root system in comparison to untreated control [Windham et al., 1989]. Suppression
of root-knot nematodes and improvement in plant growth of cardamom in nurseries has been reported
with T. harzianum [IISR, 1995]. Eapen and Venugopal [1995] have shown that isolates of Trichoderma
spp. have a broad spectrum of biocontrol activity against a number of pathogenic fungi and nematodes.
The culture filtrate of Trichoderma spp. also showed nematicidal properties [IISR, 1995].
Sharon et al. [2009] recorded enhanced parasitism of Trichoderma asperellum-203 and
Trichoderma atroviride on nematode egg masses, eggs and juveniles was enhanced when antibodies
[monoclonal and polyclonal] were incorporated into in vitro parasitism bioassays [Sharon et al., 2009].
Improved parasitism could be due to bilateral binding of the antibodies to the nematodes and conidia,
enabling better conidial attachment to the nematodes. Enhanced germination of antibody-bound conidia
further improved parasitism. Differences were observed among antibodies in their effects on fungal
parasitism and their interaction with Trichoderma species. Antibody binding to juveniles affected their
movement and viability, especially gelatinous matrix-originated juveniles. The fucose-specific lectin
Ulex europaeus-I enhanced conidial attachment to nematode life-stages. In vitro application of
Trichoderma isolates [MT-20 and S2] parasitized R. similis [zum Felde, 2002; Carñizares Monteros
2003]. Pocasangre et al. [2007] evaluated the antagonistic potential of two strains of endophytic fungus,
T. atroviride, towards the burrowing nematode, Radopholus similis, in plantain under field conditions.
The two strains were nematode suppressive. Evaluation for nematode damage was carried out every
three months after planting in the field. Single inoculation of plants with isolate MT-20 controlled R.

10
similis better than two applications of nematicides in-vitro. The results indicate possibility of replacing
nematicides with endophytes in banana.
The greenhouse and laboratory experiments revealed that T. harzianum strain BI [102–
108 spores/ml] decreased infection by M. javanica. The strain was able to penetrate the matrix leading to
a significant reduction in egg hatching. The fungus also increased the activity of peroxidase, polyphenol
oxidase and phenylalanine ammonia lyase significantly in inoculated plants [Sahebani and Hadavi,
2008]. P. lilacinus reduce galling, egg mass production, soil population and root densities compared to
control and other treatments [Zareen et al., 2001]. Cannayane and Jonathan [2008] recorded 90%
mortality of M. incognita juveniles and 80% reduction in egg hatching on application with culture
filtrate [75%] of T. viride. Bacillus subtilis, T. viride, P. chlamydosporia and P. fluorescens were also
found to be inhibitory to R. similis and P. coffeae at the same concentration. Paecilomyces lilacinus
isolates colonized M. incognita eggs and egg masses, leading to egg necrosis. Arthrobotrys oligospora
trapped M. incognita juveniles by forming hyphal networks.
19.2.3.4 Paecilomyces lilacinus [Thoms.] Samson in nematode management
Taxonomic position

Division Ascomycota
Class Deuteromycetes
Order Moniliales
Family Moniliaceae
Genus Paecelomyces

Paecilomyces species are soil-inhabiting fungus and capable of solubilizing phosphorus in soil
[Gaur, 1990]. The fungus particularly, P. lilacinus is, however, known as an aggressive parasite of eggs
and adults of nematodes [Jatala et al.,1979] It has been isolated from many cyst and root-knot
nematodes and from soil in many locations [Sterling, 1991] Several successful field trials using P.
lilacinus against pest nematodes were conducted in Peru [Sterling, 1991]. International Meloidogyne
project, led to more field trials on a variety of crops in different agroclimatic regions [Jatala, 1986].
Subsequent tests on potted plants and field plots have shown the fungus is effective in management of
numerous plant parasitic nematodes throughout the world in different crop plants [Jatala, 1985; Khan et
al., 1997]. Its effectiveness is comparable with several chemical nematicides used. The application of
MeloCon WG, a commercial product of P. lilacinus strain 251 on tomato [Burpee "Orange Pixie"
hybrid] and cucumber [Ferry-Morse"Marketmore 76"] in Hawaii protected tomato plants against
nematode damage [Schenck, 2004].
Field trials, glasshouse trials and in vitro testing of P. lilacinus continue to date and a number of
isolates have been isolated from soil, nematodes and occasionally from insects. Isolates vary in their
11
pathogenicity to plant-parasitic nematodes. Some isolates are aggressive parasites while other, though
morphologically indistinguishable, are less or non-pathogenic. Sometimes isolates which looked
promising in vitro or in glasshouse trials have failed to provide control in the field [Khan et al., 2006].
The application of P. lilacinus alone on in combination with neem leaves suppressed the root-knot
nematode on okra. The reproductive rate decreased by 24 and 46% leading to 14.8% increase in yield
over control. Ashraf and Khan [2008] evaluated the efficacy of fruit wastes of apple [Malus pumila],
banana [Musa paradisiaca], papaya [Carica papaya],pomegranate [Punica granatum] and sweet orange
[Citrus sinesis] @ 20g/plant and P. lilacinus @ 2g [mycelium+spores]/plant, alone and in combination
against reniform nematode, Rotylenchulus reniformis on chickpea under glasshouse conditions. The
individual applications of fruit wastes of sweet orange and fungal biocontrol agent P. lilacinus
significantly reduced the nematode multiplication, ultimately leading to increase in plant growth. The
best protection of chickpea against R. reniformis was recorded on integration of P. lilacinus with fruit
wastes of papaya followed by apple and pomegranate.
19.3. PHOSPHATE-SOLUBILIZING BACTERIA IN NEMATODE MANAGEMENT
There are numerous bacteria which play important role in the mineral solubilization in soil,
important species belonging to genera Azotobacter, Beijerinkia, Bacillus, Pseudomonas etc. These
bacteria are also known to suppress plant nematodes [Khan et al., 2005b]. Among the phosphate-
solubilizing bacteria, Pseudomonas and Bacillus are widely used in nematode management [Table 2].
These bacteria not only suppress the nematode pathogenesis but also promote the plant growth by
solubilizing the minerals in soil [Campbell, 1989; Wei et al., 1996; Sikora, 1988; Khan and Khan, 1998;
Khan and Tarannum, 1999; Khan et al., 2001; Siddiqui and Shaukat, 2004].
Table 2. Effect of different phosphate-solubilizing bacteria on plant parasitic nematode infesting
agricultural crops

Phosphate solubilizing bacteria Nematode managed Host plant Reference

Azospirillum lipoferum M. incognita Greengram Khan and Kaunsar, [2000]
Azotobacter chroococcum M. incognita Greengram Khan and Kaunsar, [2000];
Khan et al., [2002]
Bacillus subtilis M. incognita, M. Sugar beet Sikora, [1988], Khan and
arenaria and Tarannum, [1999]; El-
Rotylenchulus Sherief and Barakat, [1995]
reniformis. M.
incognita
Heterodera zeae
B. subtilis. M. incognita Tomato Gautam et al. [1995], Khan
and Akram, [2000]
B. subtilis M. incognita, M. Sugar beet Sikora [1988]
arenaria and
12
 Rotylenchulus
B. subtilis M. incognita Chickpea Siddiqui and Mahmood,
[1995a]
B. subtilis Heterodera cajani Pigeonpea Siddiqui and Mahmood,
[1995b]
B. subtilis M. incognita Mungbean Khan and Kounsar, [2000],
Khan et al., [2002]
B. firmus M. incognita Tomato Terefe et al., [2009]
B. subtilis M. incognita Ornamental Khan et al., 2005b
Beijerinkia indica M. incognita Greengram Khan and Kaunsar, [2000];
Khan et al., [2002]
Pseudomonas fluorescens Heterodera schachtii Sugar beet Oostendrop and Sikora
[1989]
P. fluorescens M. incognita Mungbean Khan and Kounsar, [2000],
Khan et al., [2002]
P. fluorescens of Hirschmanniella Rice Seenivasan and Devrajan,
gracilis [2000]
Pseudomonas aeruginosa strain M. javanica Tomato Siddiqui and Shaukat,
IE-6S+ and Pseudomonas [2002]; Siddiqui and
fluorescens strain CHA0 Shaukat, [2003]
P. fluorescens CHA0 or Meoloidogyne spp. Mungbean roots
Hamid et al., [2003]
CHA0/pME3424 compared with
the
P. fluorescens, P. lilacinus and Globodera Potato Seenivasan et al., [2007]
T.T. viride rostochiensis and G.
pallid
P. fluorescens [EPS291 and M. javanica Banana Rodríguez-Romero et al.,
EPS817 [2007]
P. fluorescens Meoloidogyne spp. Brinjal Anita and Rajendran [2002]
P. fluorescens [PS 07] and T. M. incognita Gladiolus Khan and Mustafa, [2005]
harzianum [T014]
P. fluorescens CHA0 or Meloidogyne species Mungbean Hamid et al., [2003]
CHA0/pME3424
P. fluorescens and T. harzianum M. javanica Tomato Siddiqui and Shaukat [2004]

19.3.1 Mechanism of nematode suppression by the phosphate-solubilizing bacteria

The phosphate solubilizing bacteria may suppress nematode pathogenesis and decrease their soil
populations through one or all of the mechenisms explained below.
19.3.1.1 Rhizosphere competence and colonization
Rhizosphere competence describes the relative root colonizing ability of a rhizobacteria [Weller
and Thomashow, 1994]. The bacteria may get attached to roots with the help of pili as in case of
Pseudomonas fluorescens on wheat roots [Vesper, 1987] or its colonization may involve development
and multiplication on root surface, however, endophytic colonization of root is also known and the
degree of colonization depends on bacterial strain and plant type. Endophytic growth of Bacillus

13
polymyxa Pw-ZR and Pseudomonas fluorescens Sm3-RN in roots has been recorded on spruce
[Shishido et al., 1999], Bacillus strain L324-92R12 and P. fluorescens 2-79RN10 on wheat [Kim et al.,
1997] and other strains on pea [Benhamou et al., 1996a, b; M’ Piga et al., 1997]. P. fluorescens CHAO
grow endophytically on tobacco [Troxler et al., 1997] and P. fluorescens WCS417r on tomato [Duijff et
al., 1997].
19.3.1.2 Antibiosis
In addition to metal chelaters and enzymes numerous antifungal metabolites are produced by
bacteria that act against nematodes both in vitro and in vivo. These include bacillomycin [Peypoux et al.,
1980, Chevanet et al., 1985], iturin [Delcambe et al., 1975; Peypoux et al., 1978; Phister et al. 2004;
Mahadtanapuk et al., 2007], surfactin, mycosubtilin [Peypoux et al., 1986], bacilysin [Roger et al.,
1965; Loeffler et al., 1986; Phister et al. 2004] fengymycin [Roger et al., 1965; Loeffler et al., 1986],
mycobacillin [Majumdar and Bose, 1970; Mannanov and Sattarova, 2001], ammonia, butyrolactones,
2,4-diacetylphloroglucinol, HCN, kanosamine, oligomycin A, oomycin A, phenazine-1-carboxylic acid,
pyoluterin, pyrrolnitrin, viscosinamide, xanthobaccin and zwittermycin A etc. [Milner et al., 1996; Keel
and Defago, 1997; Whipps, 1997a; Nielson et al., 1998; Kang et al., 1998; Kim et al., 1999; Thrane et
al., 1999; Nakayama et al., 1999].
19.3.1.3 Induced systemic resistance
Induced resistance may be defined as the process of active resistance dependent on the host
plant’s physical or chemical barriers activated by biotic and abiotic agents [Kloepper et al., 1992]. Most
of the work has focused on the systemic resistance induced by non-pathogenic rhizosphere colonizing
Bacillus and Pseudomonas species in systems where the inducing bacteria and the challenging pathogen
remain spatially separate for the duration of the experiment, and no direct interaction occurs between the
bacteria and pathogen [Sticher et al., 1997; van Loon, 1997]. Application of IE-6S+ to one half of the
split-root system caused a significant [42%] while it was 29% with CHA0 strain. The application of P.
fluorescens CHA0 or CHA0/pME3424 applied in conjunction with ammonium molybdate caused
greater reduction in nematode penetration on mungbean roots compared with the bacterial application
alone [Hamid et al., 2003]. The full range of inducible moieties produced by bacteria is probably not yet
known, but lipopolysaccharides [Leeman et al., 1995] and Siderophores [Metraux et al., 1990; Leeman
et al., 1996b] are clearly indicated. Van Peer and Schippers [1989] demonstrated that
lipopolysaccharides [LPS] extracted from the outer membrane of P. fluorescens WCS417 induced
systemic resistance in carnation against Fusarium wilt. Following changes may take place in plant roots
exhibiting induced systemic resistance as a result of inoculation with biocontrol bacteria: [i]
strengthening of epidermal and cortical cell walls and deposition of newly formed barriers beyond
14
infection sites including cellulose, lignin and phenolics [Benhaumou et al., 1996a, b, c, 2000; Duijff et
al., 1997; Jetiyanon et al., 1997; M’ Piga et al., 1997] [ii] increased levels of enzymes such as chitinase,
peroxidase, polyphenol oxidase and phenylalaline ammonia lyase [M’Piga et al., 1997; Chen et al.,
2000] [iii] enhanced production of phytoalexins [van Peer et al., 1991; Ongena et al., 1999] and [iv]
enhanced expression of stress related genes [Timmusk and Wagner, 1999]. However, all these changes
generally do not occur in one bacterial-plant combination [Steijl et al., 1999]. Similarly, the ability of
the bacteria to colonize the internal tissue of the roots has been considered to be an important feature in
many of the bacterial root interactions involving induced systemic resistance, but is not a constant
feature [Steijl et al., 1999].
19.3.1.4 Competition for iron
Although competition between for space or nutrients has been known to exist as a biocontrol
mechanism for many years [Whipps, 1997], the greatest interest recently has involved in competition for
iron. Under iron limiting conditions, bacteria produce a range of iron chelating compounds or
siderophores which have a very high affinity for ferric iron. These bacterial iron chelators are thought to
sequester the limited supply of iron available in the rhizosphere making it unavailable to pathogens,
thereby restricting their growth [O’ Sullivan and O’Gara, 1992; Loper and Henkens, 1999]. It has been
clearly shown that the plant nutrition influences the rhizosphere microbial community [Yang and
Crowley, 2000]. As an example, B. subtilis not only produced antibiotics which suppress plant
pathogens but also siderophores and the regulation of these products by the gene lpa-14 indicate the
possibility of enhanced effectiveness of biocontrol by the manipulation of the gene [Shoda, 2000]. 2, 3-
Dihydroxybenzoylglycine [2, 3-DHBG] is known as a siderophore produced by the Gram positive B.
subtilis [Leong, 1986; Ito and Neilands, 1958; Shoda, 2000]. The strains of B. subtilis which showed a
wide suppressive spectrum on plant pathogens by producing antibiotics, also produce 2, 3-DHBG.
19.3.1.5 Plant growth promotion
The plant growth promoting activity of B. subtilis and P. fluorescens results from the
contribution of different components acting either directly or indirectly on the plant. Indirect plant
growth promotion is due to suppression of soil borne plant parasites and deleterious rhizosphere
microorganisms, whereas direct plant stimulation is mainly exerted by release of growth factors. These
microorganisms may enhance the plant growth and suppress the nemtodes present in the rhizosphere
through the following mechanisms:
19.3.1.5.1 Siderophore production
Strains of B. subtilis and P. fluorescens can synthesize siderophores that can solubilize and
sequester iron in the soil making it available to plant cells [Glick, 1995]. Co-inoculation of chickpea
15
with Pseudomonas strain CRP55b resulted in 68-115% increase in nodule formation at 80 and 100 days
after planting. Khan et al. [2002] isolated nine strains of fluorescent Pseudomonas from the rhizospheres
of wheat and chickpea and were characterized morphologically as well as biochemically for
siderophores activity. All of the strains produced siderophores and were effective in the growth of
chickpea. Powell et al. [1980] demonstrated the role of iron in crop development and reported the
presence of siderophores, particularly hydroxamate siderophore [10-7 to 10-8 M], in 67 different soils of
United States, at concentrations high enough to be useful to plant roots. Akers [1983] also detected
siderophore [schizokinen] in paddy crop, suggesting their role in plant growth. Reid et al. [1984] and
Barker et al. [1985] provided evidences that plants have an ability to incorporate Fe3+ of siderophores
into their biomass. Sharma and Johri [2003] reported that fluorescent Pseudomonas strain GRP3A
produced siderophores under iron limited conditions and increased the growth of mungbean. Johri et al.
[1997] also reported that fluorescent pseudomonad strain RBT 13 producesdsiderophores which
exhibited in vitro antagonism against several bacterial and fungal pathogens and simultaneously
increased the growth of four crops.
19.3.1.5.2 Phytohormone production
Several strains of B. subtilis and P. fluorescens synthesize phytohormones such as indole acetic
acid, gibberellins, cytokinins and zeatin that promote plant growth [Gracia de Salamone et al., 2001].
Plant growth promotion is due to production of cytokinin [Gracia de Salamone et al., 2001], vitamins
[Marek-Kazaczok and Skorupsks, 2001] and IAA [Pal et al., 2001]. Application with the bacterium
enhanced growth in tea, pigeonpea, chickpea and maize [Kumar and Bezbaruah, 1997]. Indole acetic
acid, gibberellin and zeatin have been detected in the culture medium inoculated with P. fluorescens
[Meng et al., 1998]. Application of the culture filtrate promoted wheat growth in a manner similar to
application of exogenous growth regulators. A mutant strain of P. fluorescens that overproduced IAA
stimulated the root development of blackcurrant softwood cutting [Dubeikovsky et al., 1993]. IAA
produced by P. putida strain GR12-2 was found to play a major role in the root growth [Patten and
Glick, 2002]. They primary root system of canola seedlings from seeds treated with IAA producing P.
putida GR12-2 were on an average 35-50% longer than the roots from the uninoculated seeds. In
addition, exposing mungbean cuttings to high levels of IAA by soaking them in a suspension of this
bacterial strain stimulated the formation of many, very small adventitious roots. Bacillus subtilis has also
been found as a predominant bacteria in the rhizosphere of some crops [Kloepper et al., 1992]. Yeun et
al. [1985] found that B. subtilis strain improved the growth of many plant species in steamed and natural
soils. Seed treatment with B. subtilis increased the yield of carrots by 48%, oats by 33% and peanuts
upto 37% [Weller, 1988]. B. subtilis B2g caused significant increases of plant growth of cabbage,
16
cucumber and sunflower [Marten et al., 1999]. Growth promoting effects of B. subtilis and P.
fluorescens have also been reported on tomato and chickpea crops [Khan and Akram, 1997; Khan and
Khan, 2001; Khan et al., 2004].
19.3.1.5.3 Mineral solubilization and synthesis of other compounds
Phosphorus is one of the major plant nutrients which play a key role in balanced nutrition of
plants and thereby in crop production. About 98% of the Indian soils have inadequate supply of
available phosphorus [Guar, 1987] and only 0.1% of the total P present in soil is available to plants
[Scheffer and Schachtschabel, 1992]. To avoid this deficiency, phosphatic fertilizers are added in soil.
But most of phosphorus in the fertilizers becomes insoluble making it unavailable to the crop [Gaur,
1990]. Hence, solubilization of fixed soil P through the use of microorganisms is a viable option to
augment the availability of P in easily assimilative form [Parks et al., 190; Dubey and Vaishya, 2000;
Vazaquez and Hoguin, 2000]. A number species of Bacillus [Gaur and Gaind, 1987; Kole and Hajra,
1997] and Pseudomonas [Dave and Patel, 1999; Reddy and Swami, 2000] are efficient phosphate
solubilizers. Application of Pseudomonas species increased the P uptake in chickpea by 27%
[Alagawadi and Gaur, 1988a], sorghum by 18% [Alagawadi and Gaur, 1988b], potato by 26% [Kundu
and gaur, 1980] and rice by 15% [Gaur, 1990] leading to significant increase in the crop yield. Khan and
Tarannum [1999] have reported that application of B. subtilis enhanced the uptake of nitrogen and
phosphorus in tomato plants thus improving the growth and yield of tomato. Yield of wheat was also
increased when P. straita was applied along with super phosphate and rock phosphate [Gaur et al.,
1980]. Gaur and Ostwal [1972] reported that application of B. polymyxa in the presence of rock
phosphate significantly increased the P uptake of wheat and grain and straw yield. In pot experiments
where mustard was grown at different rates of Mussoorie rock phosphate with or without P. straita, the
microorganism solubilized rock phosphate more efficiently [Dubey and Vaishya, 2000]. Reddy and
Swamy [2000] conducted field experiments on blackgram by applying phosphate solubilizing bacteria,
farm yard manure and phosphorus and found improved solubilization of inorganic phosphate
compounds and increase in seed yields. Growth promoting effects of B. subtilis and P. fluorescens have
also been reported on tomato and chickpea crops [Khan and Akram, 1997; Khan and Khan, 2001; Khan
et al., 2004].Phosphate solubilizing microorganisms produce certain organic acids which are considered
the most important mechanism of phosphorus solubilization [Illmer and Schinner, 1995; Yadav and
Dadarwal, 1997]. Three strains of P. striata have been found to produce seven acids such as malic acid,
glyoxalic acid, succinic acid, fumaric acid, citric acid, tartaric acid and ketoglutaric acid [Gaur, 1990]. A
commercial formulation, Microphos, has been developed at IARI which is being successfully used by
farmers [Gaur and Gaind, 1984]. Both B. subtilis and P. fluorescens have mechanisms for the
17
solubilization of minerals such as phosphorus that become more readily available for plant growth [Pal
et al., 2001]. They may also synthesize some low molecular mass compounds, enzymes or vitamins that
can modulate plant growth and development [Marek-kazaczuk and Skorupska, 2001].
19.3.2 Bacillus subtilis [Cohn] Prazmowski in nematode management
Systematic position
Group Gram positive endospore forming rods and cocci
Family Bacillaceae
Genus Bacillus
Species subtilis

The application of B. subtilis in sugar beet considerably reduced the infection by M. incognita,
M. arenaria and Rotylenchulus reniformis [Sikora 1988] El-Sherief et. al [1995] have isolated
Bacillus, Cornybacterium, Streptomyces and Arthobacterum species from M. incognita egg masses and
Heterodera zeae cysts. A liquid culture of these bacteria at 0.1 to 0.6% concentrations was highly toxic
to juveniles of M. incognita, R. reniformis and Tylenchulus semipenetrans. Similar effects of B. subtilis
were reported by Khan and Tarannum [1999] on root-knot disease of tomato in a field study. Another
field trial has shown suppressive effects of B. subtilis on M. incognita infecting tomato [Khan and
Akram, 2000]. Effects of seed treatment [Khan and Kounsar, 2000] and soil application [Khan et al.,
2002] with B. subtilis were investigated against root-knot nematode on green gram. The bacterial
treatment decreased the galling by 33% subsequently increasing the yield of greengram by 22%. Gautam
et al. [1995] reported that B. subtilis and P. lilacinus alone or in combination increased plant height and
weight and suppressed numbers of root galls, females, eggs and second stage juveniles [J2] on tomato in
pots containing sterilized soil. B. subtilis reduced galling and multiplication of M. incognita in chickpea
[Siddiqui and Mahmood, 1995] and of Heterodera cajani in pigeonpea [Siddiqui and Mahmood, 1996]
and increased the plant growth in both the crops. Gautum et al. [1995] found that the addition of green
manure, Eiechornia crassipes to the mixture of P. lilacinum and B. subtilis enhanced the plant growth of
nematode inoculated plants. Further, a non-cellular extract of B. subtilis was also reported to have a high
degree of larvicidal properties to Heterodera cajani [Gokte and Swarup, 1988]. BioNem a commercial
formulation of B. firmus is available in the form of wettable powder [WP] and has shown great potential
for the management of root-knot nematode, M. incognita under laboratory, greenhouse and field
conditions on tomato plants. BioNem as an aqueous suspension reduced egg hatching from 98% to
100%, 24-days after treatment at 0.5%, 1%, 1.5% and 2% concentration in laboratory. Treatment of
second-stage juveniles with 2.5% and 3% concentration of BioNem, caused total inhibition of mobility,
24 hour after treatment. In the green house trials its application @ 8 g/pot reduced gall formation on
tomato seedlings by 91%, final nematode populations by 76% and the number of eggs by 45% and
18
subsequently increased the root and shoot weight [Terefe et al., 2009]. It has been found that application
of B. subtilis can also control root-knot problem of seasonal ornamental plants [Khan et al., 2005b].
19.3.3 Pseudomonas fluorescens [Threvesan] Migula in nematode management
Systematic position
Group Gram negative aerobic rods and cocci
Family Pseudomonadaceae
Genus Pseudomonas
Species fluorescens

Oostendrop and Sikora [1989] found that eight isolates of bacteria with three of them being
identified as P. fluorescens from rhizosphere of sugar beet suppressed early root infection by
Heterodera schachtii when applied to seed in non-sterilized field soil in the green house. In the field, all
isolates reduced nematode penetration with some reducing nematode number in roots by as much as
75%. Root-dip treatment of rice seedlings with P. fluorescens effectively reduced the plant damage and
population of Hirschmanniella gracilis [Seenivasan and Devrajan, 2000]. Amendment of culture filtrate
or methanol extract of the culture filtrate of a T. harzianum strain Th 6 to P. fluorescens growth medium
enhanced the production of nematicidal compound [s] by bacterial inoculants in vitro. The rhizobacteria
P. aeruginosa [strain IE-6S+] and P. fluorescens [strain CHA0] when used as bare root-dip treatment or
as soil drench application substantially reduced M. javanica penetration in tomato roots under
glasshouse conditions [Siddiqui and Shaukat, 2002; Siddiqui and Shaukat, 2003]. Application of IE-6S+
to one half of the split-root system caused a significant [42%] while it was 29% with CHA0 strain. The
application of P. fluorescens CHA0 or CHA0/pME3424 applied in conjunction with ammonium
molybdate caused greater reduction in nematode penetration on mungbean roots compared with the
bacterial application alone [Hamid et al., 2003]. The in vitro study showed inhibitory/lethal effect of
culture filtrate of P. fluorescens on M. javanica juveniles [Hamid et al., 2003]. The experiment on
efficacy of three bio-control agents viz., P. fluorescens, P. lilacinus and T. viride against potato cyst
nematodes [PCN], Globodera rostochiensis and G. pallida under field conditions revealed that the
application of P. lilacinus [7 × 108 CFU/g] @ 10 kg/ha and P. fluorescens [15 × 108 cfu/g] @ 10 kg/ha
reduced the penetration by 68.2 and 63.4%, respectively over control and also resulted in increase the
tuber yield by 88.2 and 76.2% [Seenivasan et al., 2007]. P. fluorescens [EPS291 and EPS817] @
108 CFU/g−1 substrate significantly increased aerial fresh weight, plant length and leaf area in banana.
The population of M. javanica showed a marked decline 135 days after the second treatment with the
bacteria [Rodríguez-Romero et al., 2007]. Oyekanmi, et al., [2008] observed reduction in nematode
density by 79.6% and improvement in plant growth by 46% on application with Trichoderma

19
pseudokoningii, T. viride, P. lilacinus, A. niger, Glomus mosseae and Pseudomonas fluorescens and P.
putida.
Siddiqui et al. [2003] reported that the culture filtrates of P. fluorescens strain CHAO caused
significant mortality [46%] of M. incognita juveniles in vitro compared to control [10%]. Cell
concentrations of four strains of P. fluorescens have been found inhibitory to the hatching of eggs and
survival of larvae of M. incognita [Channppa et al., 2008]. A cell concentration of 1010 of the bacterium
caused significant decrease in the hatching and induced 50% juvenile mortality. Anita and Rajendran
[2002] reported a significant reduction in nematode population, number of egg masses and gall indices
in tomato and brinjal plants in nursery plots where talc based formulation of P. fluorescens with CFU 7
x 108/g was applied @10 g/m2 of plot. Siddiqui and Ehteshamul-Haque [2001] reported that P.
aeruginosa [7.4 x 108 CFU/ml] caused the greatest reduction in gall formation due to M. javanica [500
J2/plant]. The cell free culture filtrate of P. fluorescens was found to be toxic to Heterodera avanea as it
showed 100% mortality within 24 hours [Kamra et al., 1999].
Sharma and Johri [2003] reported that fluorescent Pseudomonas strain GRP3A produced
siderophores under iron limited conditions and increased the growth of mungbean. The probable reason
for increase in plant growth may be the production of plant hormones or increased uptake of nutrients by
the plant [Chet et al., 1993]; suppression of one or more pathogens [Baker, 1986]; strengthening host
defense mechanisms [Zimand et al., 1996], siderophore production, increased synthesis of
phytohormones, better mineral solubilization, induce production of enzymes or vitamins that can
modulate plant growth and development [Marek-kazaczuk and Skorupska, 2001]. Seed treatment with
biopesticides [P. fluorescens, P. chlamydosporia and T. harzianum] @ 2g/kg seeds along with
commercial Rhizobium reduced the yield by 31 and 34% [P. fluorescens] and 28 and 25% [P.
chlamydosporia] of chickpea cultivar BG 256 in presence of M. incognita. The gall formation and egg
mass production was decreased by 23 and 18% [P. chlamydosporia] against 26 and 19% with
fenamiphos [Khan et al., 2005a]. Field study on some ornamental crops revealed that P.
chlamydosporia, P. fluorescens and B. subtilis suppressed the root-knot nematode population by 37, 27
and 24% respectively, leading to 7-15, 14-36 and 7-33% increase in the flower production of the tested
ornamentals [Khan et al., 2005b]. The frequency of colonization by the biocontrol agents was greatest
with P. chlamydosporia followed by B. subtilis and P. fluorescens. Khan and Mustafa [2005] evaluated
the efficacy of P. fluorescens [PS 07] and T. harzianum [T014] against M. incognita on different
cultivars of Gladeoli [Khan and Mustafa, 2005]. Application of P. fluorescens and nemacur decreased
the galling and soil population of the nematode.
19.4. MERITS AND DEMERITS
20
 The chemical pesticide or biopesticide has both the advantages and disadvantages associated
with their application. Environmental contamination and development of resistance are some of the
major problems accompanied with the use of chemical pesticides. Similarly, the use of phosphate-
solubilizing bacteria or fungi has both merits and demerits. Although, no environmental hazard is linked
with the use of biological control agents yet there are certain reasons that restrict their wide scale
application in sustainable agriculture.
Aspergillus niger, P. digitatum, Trichodertma, Paecilomyces lilacinus etc. can easily and
inexpensively be cultured and mass produced, show rhizospheric competence, have wide host range and
could be used as seed treatment. The limitation is that they, however, require a soil rich in organic
matter contents and high temperature for better performance and has to be applied in large amounts
under field conditions [106/g soil]. Furthermore, results vary with the species and density of nematodes.
In addition, there are certain strains that have shown pathogencity of Paecilomyces spp. [Kerry, 1987;
Stirling, 1991] and Trichodertma spp. [Guarro etal., 1999] to human populations. Phosphate-
solubilizing bacteria such as, Pseudomons and Bacillus species are easily mass cultured on synthetic
media and could be applied in soil or seeds. Their application may potentially reduce the plant damage
by suppressing nematode pathogenesis and stimulating the plant growth. However, the inhibitory
effects to nematode are of shorter duration; probably for this reason the PSMs are not commercially used
in nematode management.
19.5. FUTURE THRUST
The past three decades have seen a significant increase in the number of scientists working on
the biological control of nematodes. Current experience suggests that the integration of phosphate-
solubilizing microbes, nematicides and other control measures would be a feasible and viable strategy
for nematode management in the developed and developing countries of the world. The urgent need to
reduce the dependence on nematicides requires considerable amount of research and development in
order to commercialize the successful use of phosphate-dissolving organisms. The future of sustainable
agriculture relies heavily on the combination of biotechnology with traditional agricultural practices
involving crop rotation, trap crops, intercropping etc. Identification of microorganisms possessing
multiple growth promoting and pathogen suppressing potential for nematode management needs to be
explored and tested under changing environmental conditions. To acieve these goals, extensive field
trials are needed to ascertain their biocontrol potential under natural environment. Biologically-based
pest management has the potential to control crop diseases without causing damage to the environment.
19.6. REFERENCES

21
Agrios, G.N. [2005]. Plant Pathology. V Edition, Elsevier Academic Press, California, USA. pp.
922.
Akers, H. A. [1983]. Multiple hydroxanic acid microbial iron chelators [siderophores] in soil.
Science, 135, 156-159.
Alagawadi, A.R. and Gaur, A.C. [1988a]. Associative effect of Rhizobium and phosphate
solubilizing bacteria on yield and nutrient uptake of chickpea. Plant Soil, 105, 241-246.
Alagawadi, A.R. and Gaur, A.C. [1988b]. Interaction between Azospirillum brasilence and
phosphate solubilizing bacteria and their influence on yield and nutrient uptake of sorghum
[Sorhum bicolor L.]. Zentralblatt Fur Mikrobiologie, 143, 637-643.
Anita, B. and Rajendran, G. [2002]. Nursery application of Pseudomonas fluorescens for the control
of Meloidogyne incognita on tomato and brinjal. Nematologia Meditteranea 30, 209-210.
Anwer, A. and Khan, M.R. [2005]. Effects of soil isolates of Aspergillus niger for effectiveness
against root-knot–root-rot disease complex of egg plant. National Symposium on Recent
Advances and Research Priorities in Indian Nematology, 9-10 December 2005, IARI, New
Delhi. pp. 38.
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