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Bioresource Technology 54 (1995) 217-226 © 1996 Elsevier Science Limited

Printed in Great Britain. All fights reserved 0960-8524/95 $9.50 +0.00

ROLE OF PLANT SYMBIONTS IN NEMATODE MANAGEMENT: A REVIEW

Zaki A. Siddiqui* & Irshad Mahmood

Section of Plant Pathology and Nematology, Department of Botany, Aligarh Muslim University, Aligarh-202 002, India

(Received 25 April 1995; revised version received 2 September 1995; accepted 6 September 1995)

Abstract Mycorrhizal fungi increase soil nutrient and water absorption as plant symbionts. Root nodule bacteria, beside fixing atmospheric nitrogen, have the ability to produce antibiotics and phytoalexins, etc. The use of these two symbionts together appears to be more bene- ficial for plant growth than their use individually. The results of most studies indicate that mycorrhizal fungi and root-nodule bacteria generally reduce the severity of nematode diseases of various crops. There are possi- bilities for biological control of nematodes by selecting effective strains of mycorrhizal fungi and root-nodule bacteria, despite some obstacles.

Key words: Mycorrhizal fungi, nematode manage- ment, plant symbionts, root-nodule bacteria.

INTRODUCTION

Lewin (1982) defined symbionts as lodgers who pay rent and parasites as freeloaders who do not. Rh/zo- bium and mycorrhizal fungi are the two prime examples of symbionts. Generally, Rhizobium induce symbiosis only in legume hosts, while mycorrhizal fungi have this association with about 90% of vas- cular and economically important plants. The roles of these symbionts will be discussed in this review in relation to nematode management.

Mycorrhizai fungi Albert Bernard Frank in 1885 (Frank, 1885) intro- duced the Greek word 'mycorrhiza', which literally means 'fungus roots'. Mycorrhizal fungi form a sym- biotic relationship with plant roots in a similar fashion to root-nodule bacteria in legumes. The fun- gus takes carbohydrates from the plant and in return supplies the plant with nutrients, hormones, etc. There are four major types of mycorrhizae: (i) ecto- mycorrhiza, (ii) vesicular-arbuscular mycorrhiza (VAM), (iii) ericoid mycorrhiza, (iv) orchidaceous mycorrhiza. Ecto-mycorrhiza are commonly found on the roots of forest trees and form a thick mantle covering the outside of the roots. Inside the roots,

* Author to whom correspondence should be addressed. 217

they are present in intercellular spaces and form a characteristic structure called 'harting net'. Ericoid mycorrhizae are associated with heath plants like blueberries, azaleas, Rhododendron, etc. Orchida- ceous mycorrhizal fungi are associated with orchids.

Vesicular-arbuscular mycorrhizal (VAM) fungi are found to occur on roots of most of the food and horticultural crops and tropical trees. The presence of vesicles and arbuscules is the diagnostic criterion for identifying VAM fungi in a root. VAM fungi improve plant growth through improved uptake of nutrients, especially phosphorus. They also improve uptake of minor elements like zinc and copper and of water. They also produce plant hormones and increase the activity of nitrogen-fixing organisms. VAM fungi have been observed in 1000 genera of plants, representing some 200 families (Bagyaraj, 1991). There are at least 300 000 receptive hosts in the world flora. According to Gerdemann (1975), it is easier to list plant families that do not form VAM than to list those that do. All the VAM fungi are grouped in a single family, the Endogonaceae. The family is considered to be in an order of its own, the Endogonales, tentatively placed in the class Zygomy- cetes in the subdivision Zygomycotina (Benjamin, 1979). The seven genera, Endogone, Glomus, Scler- ocystis, Entrophospora, Acaulospora, Scutellospora and Gigaspora, presently constitute Endogonaceae. Of these only Endogone form zygospores, while others probably lack sexual reproduction. Species of Endogone do not form VAM associations. The other six genera form VAM associations.

Root-nodulating bacteria Symbiotic nitrogen fixation is not confined to the legumes only, some non-legume angiosperms also form root-nodules when invaded by soil actinomy- cetes (Callaham et aL, 1978). Allen and Allen (1947) showed that 11.8% of Mimosoideae, 3.3% of Cae- salpinioideae and 84-9% of Papilionoideae had nodules. However, another estimate showed that the nodulation status of legumes ranges from 25 to 30% for Caesalpinioideae, 60-70% for Mimosoideae and 90-95% for Papilionoideae (Lin & Burton, 1982). The ability of legumes and non-legumes to draw

218 Z. A. Siddiqui, I. Mahmood

atmospheric nitrogen is dependent on the presence of soil microorganisms of particular groups; Rhizo- biacea (Jordan, 1984) and Frankia (Lechevalier & Lechevalier, 1989). The rhizobiaceae includes two genera of root-nodule bacteria; Rhizobium Frank 1889 and Bradyrhizobium Jordan 1982. Members of the genus Rhizobium produce fast growth on yeast extract-mannitol agar and acid reaction in mineral salt-mannitol medium. Members of the genus Brady- rhizobium produce slow growth and alkaline reaction in these media. Rhizobia are aerobic rods and non- spore-forming. Frankia Brunchorst 1886 also readily infect suitable host plants, giving rise to nitrogen- fixing nodules on the roots (Callaham et al., 1978). Legumes stimulate rhizobia much more than other rhizosphere microorganisms (Nutman, 1965). Rhizo- bial nodulation is a complex symbiotic process between host plant and rhizobia. The plant provides an energy source and ecological niche for the bacteria and the bacteria provide a source of fixed nitrogen for the plant (Vance & Johnson, 1981).

INTERACTION OF MYCORRHIZAL FUNGI AND NEMATODES

Mycorrhizal fungi and plant parasitic nematodes are commonly found inhabiting the rhizosphere and colonizing the roots of their host plants. These two groups of microorganisms exert opposite effects on plant growth (Hussey & Roncadori, 1982; Schenck, 1981). A large number of reviews and chapters have appeared on the interaction of nematode and mycorrhizal fungi (Bagyaraj, 1984; Jalali & Jalali, 1991; Khan, 1993; Paulitz & Linderman, 1991). As a result of interactions, in general, the severity of nematode diseases is reduced in mycorrhizal plants (Table 1). However, in some instances root coloniza- tion by mycorrhizal fungi had no effect on nematode reproduction (Table 2), while it was even found to be stimulated in some cases (Table 3).

Reasons for reduction of nematode reproduction by mycorrhizal fungi Some of the possible reasons of reduced nematode reproduction caused by mycorrhizal fungi are as fol- lows.

Nematode parasitism by VAM fungi In some studies, parasitism of nematodes eggs with VAM fungus has been demonstrated, but the level of parasitism was not considered sufficient to nega- tively affect nematode activities (Francl & Dropkin, 1985). VAM fungal chlamydospores have been reported to occupy seeds and dead insects in soil (Rabatin & Rhodes, 1982; Taber, 1982) and have limited saprophytic capabilities (Harley & Smith, 1983). It seems likely that the VAM fungi colonize only stressed or weakened nematode eggs. The nematode parasitism by VAM fungi is opportunistic

and depends on carbon nutrition from autotrophic symbionts, rather than being representative of a true host-parasite relationship.

Changes in root morphology The colonization by mycorrhizal fungi as host-symbi- ont results in morphological changes, leading to formation of an ecto-, ericoid-, orchidaceous- or vesicular-arbuscular-mycorrhizal relationship. In the case of ectomycorrhizae, the plant root morphology changes dramatically from the non-mycorrhizal state, resulting in loss of root hairs, the development of a thick fungal mantle surrounding the epidermis and cortex and the development of extensive root branching. The increased root branching and hyphal network greatly increase the absorptive surface area (Linderman, 1988). The development of endomycor- rhizae results in loss of root hairs, but no external hyphal mantle forms, except for the relatively sparse external hyphae that occur at the rhizoplane and extend out into the surrounding soil. Roots offer structural support to the plant, function in absorp- tion of water and mineral nutrients, are the site of production of growth regulaters, are a site of starch storage and provide a nutrient supply for a wide range of microorganisms (Curl & Truelove, 1986; Rovira, 1985). Change in root morphology will ulti- mately affect their responses to other organisms. Dehne (1982) found that mycorrhizal fungi reduced disease response to plant pathogens, due to some morphological changes in the plant. Mycorrhizal plants also have a strong vascular system, which imparts greater mechanical strength to diminish the effects of pathogens (Schonbeck, 1979).

Histopathological changes Histopathological studies on galls caused by the nematode Meloidogyne ineognita showed that galls in mycorrhizal plants had fewer of the giant cells and syncytia, which are needed for the development of nematode larvae, than did non-mycorrhizal plants. Nematodes in mycorrhizal plants were smaller and took a longer time to develop into adults (Suresh, 1980). Smaller syncytia and fewer giant cells have been reported to confer resistance against nema- todes on the host plant (Trudgill & Parrott, 1969; Fassuliotis, 1970).

Physiological and biochemical changes The physiological changes caused by mycorrhizal fungi in the host plant generally reduce the severity of nematode diseases (Dehne, 1982). Phenolic com- pounds have been shown to be formed after mycorrhizal colonization (Sylvia & Sinclair, 1983) and have been thought to play a role in disease resistance (Goodman et al., 1967). Production of phytoalexin was greater on mycorrhizal roots than on non-mycorrhizal roots (Morandi, 1987) and phytoalexin is believed to play a major role in the host defenee system against pathogens (Kaplan et

Plant symbiotics in nematode control: a review 219

al., 1980). An increase in lignin and phenols in mycorrhizal plants was observed and was associated with reduced nematode reproduction (Singh et al.,

1990; Umesh et al., 1988). Increased phenylalanine and serine in tomato roots due to inoculation with VAM fungi has been observed (Suresh, 1980). These

Table 1. Mycorrhizal fungi had adverse effect on nematode reproduction

Host plant Nematode Mycorrhizal ~ngi Effect of interaction on nematodes Reference

Tobacco Meloidogyne incognita Endogone mosseae

Tobacco, M. incognita M. hapla E. mosseae oat, tomato

Tomato M. incognita Glomus mosseae

Tomato M. incognita M. javanica Glomus fasciculatum

Citrus Tylenchulus Glomus mosseae semipenetrans

Soybean M. incognita Glomus macrocarpum

Tomato Rotylenchulus Glomus fasciculatum reniformis

Cotton M. incognita Glomus etunicatum G. mosseae

Peach M. incognita Gigaspora n'uugarita Cotton M. incognita Glomus fasciculatum

Cotton M. incognita Glomus intraradices

Cotton M. incognita

Alfalfa M. hapla

Tomato, M. hapla white clover

Bean M. javanica

Tamarillo M. incognita

Cowpea Heterodera cajani

Tomato M. javanica

Pine Pratylencus penetrans Chickpea M. javanica

Cowpea Heterodera cajani

Banana Radopholus similis

G. intraradices

Mixed inoculum

Mixed inoculum

Glomus etunicatum

Mixed inoculum

Glomus fasciculatum

Glomus fasciculatum

Ectomycorrhizae Glomus manihotis Gigaspora margarita Gigaspora gigantea

Glomus fasciculatum G. epigaeus

Glomus fasciculatura

Citrus Radopholus citrophilus Glomus intraradices Soybean M. incognita Gigaspora margarita Pepper M. incognita Glomus fasciculatum

G. etunicatum

Black pepper M. incognita

Soybean Heterodera glycines

Tomato M. javanica Pigeonpea Heterodera cajani Pigeonpea H. cajani

Glomus mosseae Acaulospora laevis Glomu~ fasciculatum Gigaspora margarita Mixed inoculum

Glomus fasciculatum Glomus fasciculatum Gigaspora margarita

Had antagonistic effect on nematode population Fewer nematode larvae develop into adults in plants pre-inoculated with E. mosseae Nematode development was reduced by mycorrhizal colonization Reduced number and size of root-knot galls on mycorrhizal plants Disease symptoms were less severe on mycorrhizal plants Reduced number of galls per gram root caused by nematodes Adversally affected nematode reproduction Nematode eggs per gram root was lower on mycorrhizal plants Suppressed nematode reproduction Sixty or more spores of VAM fungi had adverse effect on nematode reproduction Adverse effect on nematode reproduction at both intervals (planting and after 28 days) Nematode population was reduced after 28 days of inoculation Reduced nematode number and adult development Number of J2 and adults per gram of root were always lower in mycorrhizal treatments Severity of nematode disease is reduced on mycorrhizal plants Suppress reproduction and development of nematodes Adverse effect on nematode reproduction Reduced nematode reproduction in plants pre-inoculated with VAM Penetration was inhibited Reproduction was differentially suppressed, most pronounced with G. manihotis, less with G. margarita and slightly with G. gigantea Prior inoculation of VAM fungi adversely affected nematode penetration more than simultaneous inoculation Nematodes were lower on mycorrhizal plants when applied simultaneously for 7 days after mycorrhizal inoculation Reduced nematode reproduction Suppressed nematode reproduction Significantly reduce galling and nematode population when pre-inoculated with VAM fungi Individually all the VAM fungi reduced nematode reproduction but the highest reduction wa s caused by A. laevis Increase tolerance to nematode in greenhouse experiment and outdoor microplots Nematode population was inhibited Reduced nematode multiplication Adverse effect on nematode reproduction

Baltruschat et al. (1973)

Sikora & Schonbeck (1975)

Sikora (1978)

Bagyaraj et al. (1979)

O'Bannon et al. (1979)

Kellam & Schenck (1980)

Sitaramaiah & Sikora (1982)

Hussey & Roncadori (1982)

Strobel et al. (1982) Saleh & Sikora (1984)

Smith et al. (1986a)

Smith et al. (1986b)

Grandison & Cooper (1986)

Cooper & Grandison (1986)

Zombolin & Oliveira (1986)

Cooper & Grandison (1987)

Jain & Sethi (1987)

Morandi (1987)

Marks et al. (1987) Diederichs (1987)

Jain&Sethi(1988)

UmeshetaL (1988)

Smith & Kaplan (1988) Carling et al. (1989) Sivaprasad et al. (1990)

Anandaraj et al. (1990)

Tylka et al. (1991)

Sundarababu et al. (1993) Siddiqui & Mahmood (1995a) Siddiqui & Mahmood (1995b)

220 Z. A. Siddiqui, L Mahmood

Table 2. Mycorrhizal fungi had no effect on nematode reproduction

Host Nematode Myeorrhizial Effect of plant fungi interaction on

nematodes

Reference

Cotton Pratylenchus brachyurus Gigaspora margarita

Citrus Radopholus similis Glomus etunicatus

Peach Meloidogyne incognita Glomus etunicatus

Tomato M. incognita Gigaspora margarita Glomus masseae

Cotton M. incognita Glomus fasciculatum

Onion M. hapla Glomus fasciculatum

Tomato M. incognita Glomus fasciculatum

Cotton M. incognita Glamus intraradices

Chickpea M. javanica Entrophospora colombiana

Musk-melon M. incognita Glomus intraradices

Reproduction was similar on mycorrhizal and non-myeorrhizal plants No effect on nematode population No effect on nematode reproduction VAM fungi had no effect on M. incognita eggs per plant or eggs per egg mass No effect on nematode reproduction up to 30 spores of G. fasciculatum No effect on nematode reproduction No difference in juvenile penetration on mycorrhizal and non-mycorrhizal plants Penetration was similar on mycorrhizal and non- mycorrhizal roots after 7 days of inoculation No effect on nematode reproduction Had no effect on the degree of root galling and number of nematodes eggs per egg mass

Hussey & Roncadori (1978)

O'Bannon & Nemec (1979)

Strobel et al. (1982)

Thompson Cason et al. (1983)

Saleh & Sikora (1984)

MacOuidwin et al. (1985)

Suresh et al. (1985)

Smith et al. (1986b)

Diederichs (1987)

Heald et al. (1989)

Table 3. Stimulatory effect of mycorrhizal fungi on nematode reproduction

Host Nematode Mycorrhizal Effect of plant fungi interation on

nematodes

Reference

Tobacco Heterodera solanacearum Endogone gigantea

Soybean Meloidogyne incognita Gigaspora heterogama Glomus macrocarpum Endogone calospora

Cotton M. incognita Gigaspora margarita

Grape M. arenaria Glomus fasciculatum

Pine Helicotylenchus Suillus luteus digonicus

Onion M. hapla Glomus fasciculatum

Cowpea Heterodera cajani Glomus epigaeus

E. gigantea increase susceptibility of tobacco to nematode Interaction was strongly influenced by species of fungal symbionts and resulted in increased nematode density Nematode reproduction was more on a per plant basis on mycorrhizal cotton because roots were larger Nematode population was highest on mycorrhizal plants Nematode population was high on mycorrhizal plants but reproduction on non- mycorrhizal plants was not measured Nematode reproduction was enhanced on mycorrhizal plants G. epigaeus stimulate nematode reproduction

Fox & Spasoff (1972)

Schenck et aL (1975)

Roncadori & Hussey (1977)

Atilano et al. (1981)

Mancini et al. (1983)

Kotcon et al. (1985)

Jain & Sethi (1987)

two amino acids are known to be inhibitory to root- knot nematodes (Reddy, 1974; Prasad, 1971).

Change in host nutrition It is a very well established fact that mycorrhizal plants contain higher concentrations of phosphorus than do non-mycorrhizal plants (Bowen, 1980; Hay- man, 1978). Improvement of phosphorus nutrition

following VAM colonization of phosphorus-deficient roots results in a decrease in membrane perme- ability and a reduction in root exudation (Graham et al., 1981). Mycorrhizal-induced decreases in root exudation have been correlated with the reduction of soil-borne diseases (Graham & Menge, 1982), while improved nutritional status of the host brought about by VAM fungus root-colonization may effect

Plant symbiotics in nematode control: a review 221

quantitative and qualitative changes in root exudates (Linderman, 1985; Reid, 1984).

The severity of nematode damage of cotton was greater on P-fertilized, non-mycorrhizal plants than mycorrhizal plants at a P level deemed adequate to high for cotton (Thompson Cason et al., 1983). This was attributed to zinc deficiency induced by nema- tode infection at high soil-P levels. High levels of P fertilization inhibit zinc uptake (Mengel & Kirkby, 1979) but apparently VAM fungi can alleviate this P-induced zinc deficiency and thus increase host tol- erance to nematode parasitism. VAM fungi have been shown to affect changes induced by environ- mental stress in root growth, root exudation, nutrient absorption and host physiology (Smith, 1988). Many of these factors are related to physiol- ogy and nutrition (Graham et al., 1981; Hayman, 1982). Changes in exudation due to P nutrition alter the chemotaxic attraction of the nematodes to roots and affect exclusion of nematode species that require a hatching stimulus (Baker & Cook, 1982). In general, VAM infection in P-deficient plants affected membrane permeability and exudation pat- terns in a way similar to that caused by P-fertilization in non-mycorrhizal plants.

Reasons for diverse results The diversity of interactions show that each nema- tode-mycorrhizal fungus-plant combination is unique and generalizations regarding such interac- tions are difficult to make. Nematode-mycorrhizal interactions are influenced by the host cultivar, nematode species, fungus species and combination, nematode and fungus initial inoculum densities, soil fertility and sequence of nematode inoculation (Smith, 1987). Most of the evidence is, however, from laboratory, greenhouse and microplot studies. There is a need for extending these studies into field conditions. Moreover, more studies are needed to confirm earlier results. Increased root growth and function, nutritional effects other than that of P, alteration in root exudation, competition for host photosynthates and competition for space and infec- tion site are some reasons which indirectly affect the host-nematode relationship in mycorrhizal plants.

INTERACTION OF ROOT-NODULE BACTERIA AND NEMATODES

The association of rhizobia with legume hosts has a beneficial effect on plant nutrition and growth. In contrast, the plant-nematode relationship has adverse effects on plant growth. The role of plant- parasitic nematodes on rhizobial nodulation and nitrogen fixation of host plants has been reviewed by a number of workers (Huang, 1987; Khan, 1993). As a result of nematode infection, the nodulation and nitrogen fixation has been reported to be suppressed (Hussaini & Seshadri, 1975), or stimulated (Hussey

& Barker, 1976), or remain unaffected (Taha & Raski, 1969). In contrast, the effect of rhizobia on plant parasitic nematodes has been studied in only a few cases (Tables 4 and 5). Inoculation of rhizobia generally had an adverse effect on nematode repro- duction (Table 4), although in a few studies inoculation has been reported to stimulate nema- tode reproduction (Table 5). The role of rhizobia in the control of plant diseases of various leguminous crops has already been discussed (Sawada, 1982) and biological control of plant diseases is now increas- ingly capturing the imagination of plant pathologists (Papavizas & Lumsden, 1980).

Reasons for the reduced nematode reproduction caused by root-nodule bacteria Some of the possible reasons for reduced nematode reproduction are as follows.

Physiological and biochemical changes The root-nodule bacteria which fix atmospheric nitrogen are reported to produce toxic metabolites inhibitory to many plant pathogens (Haque & Gaf- far, 1993) . Rhizobium japonicum secretes rhizobitoxine, which is inhibitory to charcoal root fungus, Macrophomina phaseolina (Chakraborty & Purkayastha, 1984). Chakraborty & Chakraborty (1989) reported an increased level of phytoalexin (4-hydroxy-2,3,9-trimethoxypterocarpan) when pea seeds were bacterized with Rhizobium legumino- sarum prior to inoculation with Fusarium solani f. sp. pisi. This phytoalexin may have an important role in cross-protection against many pathogens. Siddiqui and Mahmood (1994b) observed higher activity of peroxidase, nitrate reductase and catalase in pigeon- pea plants inoculated with Bradyrhizobium japonicum than in plants without B. japonicum. An increase in peroxidase activity due to B. japonicum inoculation indicates increasing resistance of the plant because it catalyzes the polymerization of phe- nolic compounds and forms cross-links between extensin, lignin and feruloylated polysaccharides (Siddiqui & Mahmood, 1994b). An increase in nitrate reductase and catalase may be correlated with the rate of protein synthesis and resistance of the plant to pathogens, respectively (Siddiqui & Mahmood, 1994b). Roslycky (1967) reported pro- duction of an antibiotic bacteriocin by rhizobia bacteria. Some properties of antibiotics of rhizobia bacteria have also been reported by others (Drapeau et al., 1973; Schwinghamer & Belkengren, 1968; Tu, 1978; Tu, 1988). Antibiotics and phytoalexin pro- duced by rhizobia bacteria probably reduce damage from nematodes and other pathogens.

Change in host nutrition Damage to plant growth by nematodes can be less- ened by the application of nitrogen fertilizer (NH4, NOa) (Ross, 1969), indicating that combined nitro- gen can improve growth of diseased plants.

222 Z. A. Siddiqu~ I. Mahmood

Combined nitrogen, such as nitrate, at a high level is a powerful inhibitor of nodulation (Dart, 1977; Pate, 1977) and also has an adverse effect on the develop- ment of nematodes (Barker et al., 1972). Barker and Huisingh (1970) observed necrosis in nodular tissues following invasion by nematodes; this may in part account for reduced nematode development. All this suggests that application of rhizobia bacteria which increase nitrogen content and plant growth can also reduce nematode populations.

Histopathological changes Endo (1964) indicated that nematodes, especially males, often caused plant necrosis and degeneration

of syncytia as the nematodes matured. Endo (1965) found that nematodes induced much necrosis in resistant plants. Some reactions that he observed were very similar to those of nodular tissues where the surrounding tissues, as well as the nematode, died. This type of reaction may partially explain the reduced number of nematodes obtained when nema- todes and Rhizobium were added simultaneously to soybean (Barker et al., 1971).

CONCLUSIONS A N D FUTURE PROSPECTS

Mycorrhizal fungi increase soil nutrients and water absorption as plant symbionts: the protection of

Table 4. Inhibitory effect of root-nodule bacteria on nematode reproduction

Host Nematode Nodulating Effect of plant bacterium interaction on

nematode

References

Soybean Heterodera g!ycines Rhizobium japonicum Reduced nematode reproduction

Soybean H. glycines R. japonicum Nodular tissues are unsuitable for nematode development and most nematodes matured as males

Mung Meloidogyne javanica Rhizobium sp. Reduced nematode multiplication

Cowpea M. incognita Rhizobium sp. Reduced nematode reproduction

Mungbean M. incognita Rhizobium sp. Prior inoculation of Rhizobium resulted in reduced nematode multiplication than simultaneous inoculation

Cowpea M. incognita Rhizobium sp. Reduced nematode Rotylenchulus reniformis multiplication

Mungbean M. incognita Rhizobium phaseoli Treatment of R. phaseoli reduce nematode reproduction

Chick pea M. incognita Bradyrhizobium sp. Reduced nematode multiplication

Lentil M. incognita Rhizobium sp. Reduced nematode R. reniformis reproduction

Chickpea M. javanica Bradyrhizobium sp. Reduced nematode R. reniformis reproduction

Pigeonpea Heterodera cajani B. japonicum Reduced nematode reproduction

Pigeonpea H. cajani B. japonicum Caused greater reduction in nematode multiplication in the presence of VAM fungi

Pigeonpea H. cajani B. japonicum Adverse affect on M. incognita nematode reproduction

Barker et al. (1971)

Barker et al. (1972)

Bopaiah et al. (1976)

Sharma & Sethi (1976)

Hussaini & Seshadri (1975)

Khan & Husain (1988)

Tiyagi & Alam (1988)

Siddiqui & Husain (1992)

Fazal et al. (1992)

Siddiqui & Mahmood (1994a)

Siddiqui & Mahmood (1994b)

Siddiqui & Mahmood (1995a)

Siddiqui & Mahmood (1995c)

Table 5. Stimulatory effect of root-nodule bacteria on nematode reproduction

Host Nematode Nodulating Effect of plant bacterium interaction on

nematodes

References

Cowpea Meloidogyne incognita Rhizobium leguminosarum Resulted in greater Ali et al. (1981) nematode multiplication

Cowpea M. incognita Rhizobium sp. Greater nematode Vashney (1982) multiplication

Mungbean, cluster-bean Heterodera cajani Rhizobium sp. Resulted in increased Dalai & Bhatti (1989) nematode reproduction

Plant symbiotics in nematode controk a review 223

roots from nematodes and other pathogens is a secondary role. Schenck (1981) pointed out that mycorrhizae offer an alternative to chemical control and we should pursue their potential as biocontrol agents. The main obstacle is to produce large quan- tities of inoculum because of their obligate nature. Working on this difficulty, Bagyaraj (1992) found Chloris gayana (Rhodes grass) to be the best host, a Perlite:Soilrite mix (1:1 v/v) to be the best substrate, while the pesticides Captan and Furadan added to the pot cultures at half the recommended level checked contaminants with no effect on the mycor- rhizal fungi. Thus the technique to produce a clean mycorrhizal inoculum with high potential in a short time, and which can be supplied to farmers as 'starter cultures', has been developed. Farmers can then multiply it in their own field for inoculating crop plants. Deep furrows can be made in a small area in the field site, the furrows filled with any available straw to partially sterilize the soil, the starter inoculum added to the furrows and the fur- rows sown with sorghum or Rhodes grass. About 2 kg straw may be needed for a 1 m x 1 m plot. After 60 days, the plant tops can be harvested and used for feeding cattle and the top 6 in. of soil, along with the roots (roots chopped into small pieces), can be air-dried and used as a mycorrhizal inoculum for inoculating crop plants. This simple technology can easily be adopted by farmers, in order to raise mycorrhizal inocula and inoculate crop plants. Mycorrhizal fungi may also be used to inoculate the seedlings of certain crops. The seedlings for this pur- pose would be raised in a nursery and then placed in the field. In this way, prospects of mycorrhizal fungi as biocontrol agents can be fully assessed in the field.

The presence of rhizobia in the rhizosphere pre- sumably protects the host roots from pathogens, besides fixing atmospheric nitrogen. The use of rhi- zobia with mycorrhizal fungi is more beneficial for reducing the damage caused by pathogens (Siddiqui & Mahmood, 1995a). The use of these symbionts will reduce the damage without use of chemical pes- ticides, which are costly and have health hazards. Moreover, use of these two symbionts together will increase nitrogen and phosphorus uptakes without the application of any synthetic fertilizer. In this way, the farmers can also save the capital which they invest for fertilizers.

ACKNOWLEDGEMENTS

The senior author thanks the Council of Scientific and Industrial Research, New Delhi, for the award of a Research Associateship. The authors also thank Prof. D. J. Bagyaraj, Head, Department of Agri- cultural Microbiology, University of Agricultural Sciences, G.K.V.K. Campus, Bangalore, India, for his critical suggestions.

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