Abstract
Plant-parasitic nematodes cause significant economic losses to a wide variety of crops. Chemical control is a widely used option for plant-parasitic nematode management. However, chemical nematicides are now being reappraised in respect of environmental hazard, high costs, limited availability in many developing countries or their diminished effectiveness following repeated applications. This review presents progress made in the field of microbial antagonists of plant-parasitic nematodes, including nematophagous fungi, endophytic fungi, actinomycetes and bacteria. A wide variety of microorganisms are capable of repelling, inhibiting or killing plant-parasitic nematodes, but the commercialisation of these microorganisms lags far behind their resource investigation. One limiting factor is their inconsistent performance in the field. No matter how well suited a nematode antagonist is to a target nematode in a laboratory test, rational management decision can be made only by analysing the interactions naturally occurring among “host plant–nematode target–soil–microbial control agent (MCA)–environment”. As we begin to develop a better understanding of the complex interactions, microbial control of nematodes will be more fine-tuned. Multidisciplinary collaboration and integration of biological control with other control methods will␣also contribute to more successful control practices.
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Abbreviations
- DBCP:
-
dibromochloropropane
- EDB:
-
ethylene dibromide
- MCA:
-
microbial control agent
- PGPR:
-
plant growth-promoting rhizobacteria
References
Ahrén D, Tunlid A (2003) Evolution of parasitism in nematode-trapping fungi. J Nematol 35:194–197
Akhtar M (1997) Current options in integrated management of plant-parasitic nematodes. Integr Pest Manag Rev 2:187–197
Akhtar M, Mahmood I (1996) Control of plant-parasitic nematodes with organic and inorganic amendments in agricultural soil. Appl Soil Ecol 4:243–247
Alabouvette C (1999) Fusarium wilt suppressive soils: an example of disease suppressive soil. Australas Plant Path 28:57–64
Ali-Hazmi AS, Ibrahim AAM, Abdul-Raziq AT (1993) Evaluation of a nematode-encapsulation fungi complex for control of Meloidogyne javanica on potato. Pak J Nematol 11:139–149
Al-Hazmi AS, Schmitt DP, Sasser JN (1982) The effect of Arthrobotrys conoides on Meloidogyne incognita population densities in corn as influenced by temperature, fungus inoculum density, and time of fungus introduction in the soil. J Nematol 14:168–174
Ali NI, Siddiqui IA, Shaukat SS, Zaki MJ (2002) Nematicidal activity of some strains of Pseudomonas spp. Soil Biol Biochem 34:1051–1058
Alphey TJW, Robertson WM, Lyon GD (1988) Rishitin a natural plant product with nematicidal activity. Revue Nématol 11:399–404
Al-Rehiayani S, Hafez SL, Thornton M, Sundararaj P (1999) Effects of Pratylenchus neglectus, Bacillus megaterium and oil radish or rapeseed green manure on reproductive potential of Meloidogyne chitwoodi on potato. Nematropica 29:37–49
Anver S, Khan AA, Alam MM (2001) Integrated management of root-knot and reniform nematodes with neem cake and biocontrol fungus Paecilomyces lilacinus on chickpea and pigeonpea. Arch Phytopath Pflanz 34:255–264
Ashour EH, Mostafa FAM (1999) Effect of pollution with certain heavy metals on the growth of the nematophagous fungus, Arthrobotrys oligospora, trap formation, root-knot nematode infection and enzyme production. Pak J Biol Sci 2:515–522
Bae Y-S, Knudsen GR (2001) Influence of a fungus-feeding nematode on growth and biocontrol efficacy of Trichoderma harzianum. Phytopathology 91:301–306
Barker KR, Koenning SR (1998) Developing sustainable systems for nematode management. Annu Rev Phytopathol 36:165–205
Bourne JM, Kerry BR (1999) Effect of the host plant on the efficacy of Verticillium chlamydosporium as a biological control agent of root-knot nematodes at different nematode densities and fungal application rates. Soil Biol Biochem 31:75–84
Bourne JM, Kerry BR, de Leij FAAM (1996) The importance of the host plant on the interaction between root-knot nematodes Meloidogyne spp. and␣the nematophagous fungus, Verticillium chlamydosporium Goddard. Biocontrol Sci Technol 6:539–548
Butt TM, Jackson C, Magan N (2001) Fungal biocontrol agents-appraisal and recommendations. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems and potential.CABI Publishing, Wallingford UK, pp 27–69
Cabanillas E, Barker KR, Nelson LA (1989) Growth of isolates of Paecilomyces lilacinus and their efficacy in biocontrol of Meloidogyne incognita on tomato. J Nematol 21:164–172
Carneiro RMDG, Cayrol JC (1991) Relationship between inoculum density of the nematophagous fungus Paeeilomyces lilacinus and control of Meloidogyne arenaria on tomato. Revue Nématol 14:629–634
Cayrol JC (1983) Biological control of Meloidogyne by Arthrobotrys irregularis (in French, with English abstract). Revue Nématol 6:265–273
Chavarría-Carvajal JA, Rodríguez-Kábana R, Kloepper JW, Morgan-Jones G (2001) Changes in populations of microorganisms associated with organic amendments and benzaldehyde to control plant-parasitic nematodes. Nematropica 31:165–180
Chen J, Abawi GS, Zuckerman BM (2000) Efficacy of Bacillus thuringiensis, Paecilomyces marquandii, and Streptomyces costaricanus with and without organic amendments against Meloidogyne hapla infecting lettuce. J Nematol 32:70–77
Chen SY, Chen FJ (2003) Fungal parasitism of Heterodera glycines eggs as influenced by egg age and pre-colonization of cysts by other fungi. J Nematol 35:271–277
Chen SY, Dickson DW, Mitchell DJ (1996) Pathogenicity of fungi to eggs of Heterodera glycines. J Nematol 28:148–158
Chen SY, Reese CD (1999) Parasitism of the nematode Heterodera glycines by the fungus Hirsutella rhossiliensis as influenced by crop sequence. J Nematol 31:437–444
Cooke RC (1962) Behavior of nematode-trapping fungi during decomposition of organic matter in soil. Trans Br Mycol Soc 45:314–320
Cronin D, Moenne-Loccoz Y, Dunne C, O’Gara F (1997) Inhibition of egg hatch of the potato cyst nematode Globodera rostochiensis by chitinase-producing bacteria. Eur J Plant Pathol 103:433–440
Dabiré KR, Ndiaye S, Chotte J-L, Fould S, Diop MT, Mateille T (2005) Influence of irrigation on the distribution and control of the nematode Meloidogyne javanica by the biocontrol bacterium Pasteuria penetrans in the field. Biol Fertil Soils 41:205–211
Davies KG, Fargette M, Balla G, Daudi A, Duponnois R, Gowen SR, Mateille T, Phillips MS, Sawadogo A, Trivino C, Vouyoukalou E, Trudgill DL (2001) Cuticle heterogeneity as exhibited by Pasteuria spore attachment is not linked to the phylogeny of parthenogenetic root-knot nematodes (Meloidogyne spp.). Parasitology 122:111–120
de la Peña E, Echeverría SR, van der Putten WH, Freitas H, Moens M (2006) Mechanism of control of root-feeding nematodes by mycorrhizal fungi in the dune grass Ammophila arenaria. New Phytol 169:829–840
Dickson DW, Mitchell DJ (1985) Evaluation of Paecilomyces lilacinus as a biocontrol agent of Meloidogyne javanica on tabacco. J Nematol 17:519
Diedhiou PM, Hallmann J, Oerke E-C, Dehne H-W (2003) Effects of arbuscular mycorrhizal fungi and a non-pathogenic Fusarium oxysporum on Meloidogyne incognita infestation of tomato. Mycorrhiza 13:199–204
Doran JW, Sarrantonio M, Liebig MA (1996) Soil health and sustainability. Adv Agron 56:1–54
Dube B, Smart GC Jr (1987) Biological control of Meloidogyne incognita by Paecilomyces lilacinus and Pasteuria penetrans. J Nematol 19:222–227
Duponnois R, Bâ AM, Mateille T (1999) Beneficial effects of Enterobacter cloacae and Pseudomonas mendocina for biocontrol of Meloidogyne incognita with the endospore-forming bacterium Pasteuria penetrans. Nematology 1:95–101
Duponnois R, Mateille T, Gueye M (1995) Biological characteristics and effects of two strains of Arthrobotrys oligospora from Senegal on Meloidogyne species parasitizing tomato plants. Biocontrol Sci Technol 5:517–525
Duponnois R, Mateille T, Sene V, Sawadogo A, Fargette M (1996) Effect of different West african species and strains of Arthrobotrys nematophagous fungi on Meloidogyne species. Entomophaga 41:475-483
Eapen SJ, Beena B, Ramana KV (2005) Tropical soil microflora of spice-based cropping systems as potential antagonists of root-knot nematodes. J Invertebr Pathol 88:218–225
El-Nagdi WMA, Youssef MMA (2004) Soaking faba bean seed in some bio-agents as prophylactic treatment for controlling Meloidogyne incognita root-knot nematode infection. J Pest Sci 77:75–78
Ellis RJ, Timms-Wilson M, Bailey MJ (2000) Identification of conserved traits in fluorescent pseudomonads with antifungal activity. Environ Microbiol 2:274–284
Elsen A, Baimey H, Swennen R, De Waele D (2003) Relative mycorrhizal dependency and mycorrhiza–nematode interaction in banana cultivars (Musa spp.) differing in nematode susceptibility. Plant Soil 256:303–313
Eren J, Pramer D (1978) Growth and activity of the nematode-trapping fungus Arthrobotrys conoides in soil. In: Loutit MW, Miles JAR (eds) Microbial ecology. Springer-Verlag, Berlin, pp 121–127
Esnard J, Marban-Mendoza N, Zuckerman BM (1998) Effects of three microbial broth cultures and an organic amendment on growth and populations of free living and plant-parasitic nematodes on banana. Eur J Plant Pathol 104:457–463
Fernández C, Rodríguez-Kábana R, Warrior P, Kloepper JW (2001) Induced soil suppressiveness to a root-knot nematode species by a nematicide. Biol Control 22:103–114
Field TK, Riggs RD, Robins RT (1996) In vitro effects of cyst associated bacteria on growth of the fungal hyphomycete (ARF18) a biocontrol agent for Heterodera glycines. Nematropica 26:263
Forge T, Muehlchen A, Hackenberg C, Neilsen G, Vrain T (2001) Effects of preplant inoculation of apple (Malus domestica Borkh.) with arbuscular mycorrhizal fungi on population growth of the root-lesion nematode, Pratylenchus penetrans. Plant Soil 236:185–196
Friman E (1993) UV inhibition of the nematode infection process in Arthrobotrys oligospora and Dactylaria candida. J Gen Microbiol 139:2841–2847
Gaspard JT, Mankau R (1987) Density-dependence and host-specificity of the nematode-trapping fungus Monacrosporium elipsosporum. Revue Nématol 10:241–246
Gray (1985) Ecology of nematophagous fungi: effect of soil moisture, organic matter, pH and nematode density on distribution. Soil Biol Biochem 17:499–507
Grewal PS, Lewis ED, Venkatachari S (1999) Allelopathy: a possible mechanism of suppression of plant-parasitic nematodes by entomopathogenic nematodes. Nematology 1:735–743
Hackenberg C, Muehlchen A, Forge T, Vrain T (2000) Pseudomonas chlororaphis strain Sm3, bacterial antagonist of Pratylenchus penetrans. J Nematol 32:183–189
Hallmann J, Sikora RA (1996) Toxicity of fungal endophyte secondary metabolites to plant parasitic nematodes and soil-borne plant pathogenic fungi. Eur J Plant Pathol 102:155–162
Holland RJ, Williams KL, Khan A (1999) Infection of Meloidogyne javanica by Paecilomyces lilacinus. Nematology 1:131–139
Hu KJ, Li JX, Webster JM (1999) Nematicidal metabolites produced by Photorhabdus luminescens (Enterobacteriaceae), bacterial symbiont of entomopathogenic nematodes. Nematology 1:457–469
Huang XW, Tian BY, Niu QH, Yang JK, Zhang LM, Zhang KQ (2005) An extracellular protease from Brevibacillus laterosporus G4 without parasporal crystals can serve as a pathogenic factor in infection of nematodes. Res Microbiol 156:719–727
Hyakumachi M, Kubota M (2004) Fungi as plant growth promoter and disease suppressor. In: Arora DK, Bridge PD, Bhatnagar D (eds) Fungal biotechnology in agricultural, food, and environmental applications. Marcel Dekker Inc., New York, NY, pp 101–110
Ibrahim AAM (1994) Effect of cadusafos, Paecilomyces lilacinus and Nemout on reproduction and damage potential of Meloidogyne javanica. Pak J Nematol 12:141–147
Insunza V, Alstrom S, Eriksson KB (2002) Root bacteria from nematicidal plants and their biocontrol potential against trichodorid nematodes in potato. Plant Soil 241:271–278
Irving F, Kerry BR (1986) Variation between strains of the nematophagous fungus, Verticillium chlamydosporium Goddard. II. Factors affecting parasitism of cyst nematode eggs. Nematologica 32:474–485
Jacobs H, Gray SN, Crump DH (2003) Interactions between nematophagous fungi and consequences for their potential as biological agents for the control of potato cyst nematodes. Mycol Res 107:47–56
Jacq VA, Fortuner R (1979) Biological control of rice nematodes using sulphate reducing bacteria. Revue Nématol 2:41–50
Jaffee BA (1992) Population biology and biological control of nematodes. Can J Microbiol 38:359–364
Jaffee BA (1999) Enchytraeids and nematophagous fungi in tomato fields and vineyards. Phytopathology 89:398–406
Jaffee BA, Ferris H, Stapleton JJ, Norton MVK, Muldoon AE (1994) Parasitism of nematodes by the fungus Hirsutella rhossiliensis as affected by certain organic amendments. J Nematol 26:152–161
Jaffee BA, Gaspard JT, Ferris H (1989) Density-dependent parasitism of the soil-borne nematode Criconemella xenoplax by the nematophagous fungus Hirsutella rhossiliensis. Microb Ecol 17:193–200
Jaffee BA, McInnis TM (1991) Sampling strategies for detection of density-dependent parasitism of soil-borne nematodes by nematophagous fungi. Revue Nématol 14:147–150
Jaffee BA, Muldoon AE, Didden WAM (1997) Enchytraeids and nematophagous fungi in soil microcosms. Biol Fertil Soils 25:382–388
Jaffee BA, Zasoski RJ (2001) Soil pH and the activity of a pelletized nematophagous fungus. Phytopathology 91:324–330
Jagdale GB, Grewal PS (2002) Identification of alternatives for the management of foliar nematodes in floriculture. Pest Manag Sci 58:451-458
Jansson H-B, Jeyaprakash A, Zuckerman BM (1985) Control of root-knot nematodes on tomato by the endoparasitic fungus Meria coniospora. J Nematol 17:327–329
Jansson H-B, Lopez-Llorca LV (2001) Biology of nematophagous fungi. In: Misra JK, Horn BW (eds) Trichomycetes and other fungal groups: Robert W. Lichtwardt commemoration volume. Science Publishers Inc., Enfield, NH, pp 144–173
Jansson H-B, Tunlid A, Nordbring-Hertz B (1997) Nematodes. In: Anke T (eds) Fungal Biotechnology. Chapman and Hall, Weinheim, Germany, pp 38–48
Jatala P (1986) Biological control of plant-parasitic nematodes. Annu Rev Phytopathol 24:453–489
Jenkins NE, Grzywacz D (2000) Quality control of fungal and viral biocontrol agents-assurance of product performance. Biocontrol Sci Technol 10:753–777
Johnson AW, Burton GW, Sumner DR, Handoo Z (1997) Coastal bermudagrass rotation and fallow for management of nematodes and soilborne fungi on vegetable crops. J Nematol 29:710–716
Jonathan EI, Barker KR, Abdel-Alim FF, Vrain TC, Dickson DW (2000) Biological control of Meloidogyne incognita on tomato and banana with rhizobacteria, actinomycetes, and Pasteuria penetrans. Nematropica 30:231–240
Kerry BR (2000) Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annu Rev Phytopathol 38:423–441
Kim DG, Riggs RD (1995) Efficacy of the nematophagous fungus ARF18 in alginate-clay pellet formulations against Heterodera glycines. J Nematol 27(4S):602–608
Kimpinski J, Sturz AV (2003) Managing crop root zone ecosystems for prevention of harmful and encouragement of beneficial nematodes. Soil Till Res 72:213–221
Kobayashi DY, Palumbo JD (2000) Bacterial endophytes and their effects on plants and uses in agriculture. In: White JF, Bacon CW (eds) Microbial Endophytes. Marcel Dekker, Inc., New York, NY, pp 199–235
Kornis GI (1994) Avermectins and milbemycins. In: Godfrey CRA (eds) agrochemicals from natural products. Marcel Dekker, Inc., New York, NY, pp 215–255
Kratochvil RJ, Sardanelli S, Everts K, Gallagher E (2004) Evaluation of crop rotation and other cultural practices for management of root-knot and lesion nematodes. Agron J 96:1419–1428
Kulkarni SM, Sangita D (2000) Cultivation of Hohenbuehelia atrocaerulea (Fr.) Sing. (Agaricomycetideae): a mushroom with nematicidal potential. Int J Med Mushrooms 2:161–163
Lai YX, Li GP, Wang YH, Zhang YF, Zhou YP (2005) Trials on killing beetles of Monochamus alternatus and controlling pine wilt disease with Manic-EC and mixtures of Beauveria bassiana × Verticillium lecanii (in Chinese, with English abstract). J Jiangsu For Sci Technol 32:4–7
Lay EC, Lara J, Jatala P, Gonzales F (1982) Preliminary evaluation of Paecilomyces lilacinus as a biological control of the root-knot nematode, Meloidogyne incognita, in industrial tomatoes. Nematropica 12:154
Liu ZM, Qin BX, Cai JH, Chen YH, Huang FX, Zhu GN, Lu XH (2005) The effects of soil factors on bacterium B2’s control of Meloidogyne incognita (in Chinese, with English abstract). J Huazhong Agric Univ 24:161–164
Lohmann U, Sikora RA, Hofer M (1989) Influence of phosphoiipids on growth, sporulation and virulence of the endoparasitic fungi Drechmeria coniospora, Verdcillium balanoides and Harposporium anguillulae in liquid culture. J Phytopathol 125:139–147
López-Llorca LV, Boag B (1990) Inhibition of Verticillium suchlasporium and other nematophagous fungi by bacteria colonising Heterodera avenae females. Nematol Mediterr 18:233–237
López-Llorca LV, Duncan GH (1991) Effects of fungal parasites on cereal cyst nematodes (Heterodera avenae Woll.) from naturally infested soil—a scanning electron microscopy study. Can J Microbiol 37:218–225
López-Llorca LV, Olivares-Bernavéu C (1997) Growth inhibition of nematophagous and entomopathogenic fungi by leaf litter and soil containing phenols. Mycol Res 101:691–697
Luo H, Mo MH, Huang XW, Li X, Zhang KQ (2004) Coprinus comatus: a basidiomycete fungus forms novel spiny structures and infects nematode. Mycologia 96:1218–1225
Mankau R (1980) Biological control of nematode pests by natural enemies. Annu Rev Phytopathol 18:415–440
Mankau R, Prasad N (1977) Infectivity of Bacillus penetrans in plant-parasitic nematodes. J Nematol 9:40–45
Mateille T, Duponnois R, Diop MT (1995) Influence of abiotic soil factors and the host plant on the infection of phytoparasitic nematodes of the genus Meloidogyne by the actinomycete parasitoid Pasteuria penefrans (in French, with English abstract). Agronomie 15:581–589
McGovern RJ, McSorley R, Bell ML (2002) Reduction of landscape pathogens in Florida by soil solarization. Plant Dis 86:1388–1395
Meyer SLF, Roberts DP (2002) Combinations of biocontrol agents for management of plant-parasitic nematodes and soilborne plant-pathogenic fungi. J Nematol 34:1–8
Meyer SLF, Roberts DP, Chitwood DJ, Carta LK, Lumsden RD, Mao WL (2001) Application of Burkholderia cepacia and Trichoderma virens, alone and in combinations, against Meloidogyne incognita on bell pepper. Nematropica 31:75–86
Mian IH, Godoy G, Shelby RA, Rodríguez-Kábana R, Morgan-Jones G (1982) Chitin amendments for control of Meloidogyne arenaria in infested soil. Nematropica 12:71–84
Mittal N, Saxena G, Mukerji KG (1995) Integrated control of root-knot disease in three crop plants using chitin and Paecilomyces lilacinus. Crop Prot 14:647–651
Mondal SN, Hyakumachi M (1998) Carbon loss and germinability, viability, and virulence of chlamydospores of Fusarium solani f. sp. phaseoli agter exposure to soil at different pH levels, temperatures, and matric potentials. Phytopathology 88:148–155
Monfort E, Lopez-Llorca LV, Jansson H-B, Salinas J, Park JO, Sivasithamparam K (2005) Colonisation of seminal roots of wheat and barley by egg-parasitic nematophagous fungi and their effects on Gaeumannomyces graminis var. tritici and development of root-rot. Soil Biol Biochem 37:1229–1235
Mukerji KG, Chamola BP, Singh J (2000) Preface. In: Mukerji KG, Chamola BP, Singh J (eds) Mycorrhizal biology. Kluwer Academic/Plenum Publishers, New York, NY, VII pp
Nannipieri P, Ascher J, Ceccherini MT, Pertramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670
Neipp PW, Becker JO (1999) Evaluation of biocontrol activity of rhizobacteria from Beta vulgaris against Heterodera schachtii. J Nematol 31:54–61
Oka Y, Nacar S, Putievsky E, Ravid U, Yaniv Z, Spiegel Y (2000) Nematicidal activity of essential oils and their components against the root-knot nematode. Phytopathology 90:710–715
Okada H, Harada H, Kadota I (2005) Fungal-feeding habits of six nematode isolates in the genus Filenchus. Soil Biol Biochem 37:1113–1120
Pandey R, Sikora RA (2000) Influence of aqueous extracts of organic matter on the sensitivity of Heterodera schachtiiSchmidt and Meloidogyne incognita (Kofoid and White) Chitwood eggs to Verticillium chlamydosporium Goddard infection (in German, with English abstract). Zeitsch Pflanzenkr Pflanzensch 107:494–497
Persmark L, Marban-Mendoza N, Jansson H-B (1995) Nematophagous fungi from agricultural soils of Central America. Nematropica 2:117–124
Persson C, Jansson H-B (1999) Rhizosphere colonization and control of Meloidogyne spp. by nematode-trapping fungi. J Nematol 31:164–171
Pinochet J, Calvet C, Camprubí, Fernández C (1996) Interactions between migratory endoparasitic nematodes and arbuscular mycorrhizal fungi in perennial crops: a review. Plant Soil 185:183–190
Ploeg AT (2002) Effects of selected marigold varieties on root-knot nematodes and tomato and melon yields. Plant Dis 86:505–508
Poinar GO Jr, Georgis R (1994) Biological control for plant-parasitic nematodes attacking turf and ornamentals. In: Leslie AR (eds) Handbook of integrated pest management for turf and ornamentals. CRC Press, Boca Raton, FL, pp 491–501
Rao MS, Kerry BR, Gowen SR, Bourne JM, Reddy PP (1997) Management of Meloidogyne incognita in tomato nurseries by integration of Glomus deserticola with Verticillium chlamydosporium. J Plant Dis Prot 104:419–422
Reynolds LB, Potter JW, Ball-Coelho BR (2000) Crop rotation with Tagetes sp. is an alternative to chemical fumigation for control of root-lesion nematodes. Agron J 92:957–966
Rice EL (1984) Allelopathy, 2nd edn. Academic Press Inc., Orlando FL, 422 pp
Roberts PA, Thomason IJ, McKinney HE (1981) Influence of nonhosts, crucifers, and fungal parasites on field populations of Heterodera schochtii. J Nematol 13:164–171
Rosenzweig WD, Pramer D (1980) Influence of cadmium, zinc, and lead on growth, trap formation, and collagenase activity of nematode-trapping fungi. Appl Environ Microb 40:694–696
Ryan A, Jones P (2004) The effect of mycorrhization of potato roots on the hatching chemicals active towards the potato cyst nematodes,Globodera pallida and G. rostochiensis. Nematology 6:335–342
Samac DA, Kindel LL (2001) Suppression of the root-lesion nematode (Pratylenchus penetrans) in alfalfa (Medicago sativa) by Streptomyces spp. Plant Soil 235:35–44
Santos MAD, Ferraz S, Muchovej JJ (1992) Evaluation of 20 species of fungi from Brazil for biocontrol of Meloidogyne incognita race 3. Nematropica 22:183–192
Sasser JN, Freckman DW (1987) A world perspective on nematology: the role of the society. In: Veech JA, Dickson DW (eds) Vistas on nematology: a commemoration of the twenty-fifth anniversary of the society of nematologists. Society of Nematologists, Lakeland, FL, pp 7–14
Sasser JN, Uzzell G Jr (1991) Control of the soybean cyst nematode by crop rotation in combination with a nematicide. J Nematol 23:344–347
Sayre RM, Walter DE (1991) Factors affecting the efficacy of natural enemies of nematodes. Annu Rev Phytopathol 29:149–166
Schwarz M, Kopcke B, Weber RWS, Sterner O, Anke H (2004) 3-Hydroxypropionic acid as a nematicidal principle in endophytic fungi. Phytochemistry 65:2239–2245
Siddiqui IA, Ehteshamul-Haque S (2001) Suppression of the root rot–root knot disease complex by Pseudomonas aeruginosa in tomato: the influence of inoculum density, nematode populations, moisture and other plant-associated bacteria. Plant Soil 237:81–89
Siddiqui IA, Shaukat SS (2002) Mixtures of plant disease suppressive bacteria enhance biological control of multiple tomato pathogens. Biol Fertil Soils 36:260-268
Siddiqui IA, Shaukat SS (2003) Plant species, host age and host genotype effects on Meloidogyne incognita biocontrol by Pseudomonas fluorescens strain CHA0 and its genetically-modified derivatives. J Phytopathol 151:231–238
Siddiqui ZA (2004) Effects of plant growth promoting bacteria and composed organic fertilizers on the reproduction of Meloidogyne incognita and tomato growth. Bioresour Technol 95:223–227
Siddiqui ZA, Mahmood I (1995) Role of plant symbionts in nematode management: a review. Bioresour Technol 54:217–226
Sikora RA (1992) Management of the antagonistic potential in agricultural ecosystems for the biological control of plant parasitic nematodes. Annu Rev Phytopathol 30:245–270
Soler-Serratosa A, Kokalis-Burelle N, Rodríguez-Kábana R, Weaver CF, King PS (1996) Allelochemicals for control of plant-parasitic nematodes.1. In vivo nematicidal efficacy of thymol and thymol benzaldehyde combinations. Nematropica 26:57–71
Sorbo GD, Marziano F, D’Errico FP (2003) Diffusion and effectiveness of the nematophagous fungus Hirsutella rhossiliensis in control of the cyst nematode Heterodera daverti under field conditions. J Plant Pathol 85:219–221
Sorribas FJ, Ornat C, Galeano M, Verdejo-Lucas S (2003) Evaluation of a native and introduced isolate of Pochonia chlamydosporia against Meloidogyne javanica. Biocontrol Sci Technol 13:707–714
Stirling GR, Licastro KA, West LM, Smith LJ (1998) Development of commercially acceptable formulations of the nematophagous fungus Verticillium chlamydosporium. Biol Control 11:217–223
Stirling GR, Wachtel MF (1980) Mass production of Bacillus penetrans for the biological control of root-knot nematodes. Nematologica 26:308–312
Strobel NE, Hussey RS, Roncadori RW (1982) Interactions of vesicular–arbuscular mycorrhizal fungi, Meloidogyne incognita, and soil fertility on peach. Phytopathology 72:690–694
Sturz AV, Kimpinski J (2004) Endoroot bacteria derived from marigolds (Tagetes spp.) can decrease soil population densities of root-lesion nematodes in the potato root zone. Plant Soil 262:241–249
Stutzman-Engwall K, Conlon S, Fedechko R, McArthur H, Pekrun K, Chen Y, Jenne S, La C, Trinh N, Kim S, Zhang YX, Fox R, Gustafsson C, Krebber A (2005) Semi-synthetic DNA shuffling of aveC leads to improved industrial scale production of doramectin by Streptomyces avermitilis. Metab Eng 7:27–37
Sun SH, Zhou L, Xia ZY, Zhao YH, Duan LC (2002) Study of microorganic nematicide to control tobacco root-knot nematodes (in Chinese, with English abstract). Acta Tabacaria Sin 8:30–33
Talavera M, Itou K, Mizukubo T (2001) Reduction of nematode damage by root colonization with arbuscular mycorrhiza (Glomus spp.) in tomato-Meloidogyne incognita (Tylenchida: Meloidogynidae) and carrot-Pratylenchus penetrans (Tylenchida: Pratylenchidae) pathosystems. Appl Entomol Zool 36:387–392
Talavera M, Itou K, Mizukubo T (2002) Combined application of Glomus sp. and Pasteuria penetrans for reducing Meloidogyne incognita (Tylenchida: Meloidogynidae) populations and improving tomato growth. Appl Entomol Zool 37:61–67
Tedford EC, Jaffee JA, Muldoon AE (1994) Variability among isolates of the nematophagous fungus Hirsutella rhossiliensis. Mycol Res 98:1127–1136
Timper P, Brodie BB (1993) Infection of Pratylenchus penetrans by nematode-pathogenic fungi. J Nematol 25:297–302
Toyota K, Ritz K, Young IA (1996) Microbiological factors affecting colonization of soil aggregates by Fusarium oxysporium f. sp. raphani. Soil Biol Biochem 28:1513–1521
Twomey U, Warrior P, Kerry BR, Perry RN (2000) Effects of the biological nematicide, DiTera, on hatching of Globodera rostochiensis and G. pallida. Nematology 2:355–362
van den Boogert PHJF, Velvis H, Ettema CH, Bouwman LA (1994) The role of organic matter in the population dynamics of the endoparasitic nematophagous fungus Drechmeria coniospora in microcosms. Nematologica 40:249–257
Verdejo S, Jaffee BA (1988) Reproduction of Pasteuria penetrans in a tissue system containing Meloidogyne javanica and Agrobacterium rhizogenes transformed roots. Phytopathology 78:1284–1286
Viaene NM, Abawi GS (1998) Fungi parasitic on juveniles and egg masses of Meloidogyne hapla in organic soils from New York. J Nematol 30(4S):632–638
Waceke JW, Waudo SW, Sikora R (2001) Suppression of Meloidogyne hapla by arbuscular mycorrhiza fungi (AMF) on pyrethrum in Kenya. Int J Pest Manage 47:135–140
Walia RK, Vats R (2000) Fungal antagonists of phytonematodes. In: Upadhyay RK, Mukerji KG, Chamola BP (eds) Crop diseases, weeds, and nematodes. Kluwer Academic/Plenum Publishers, New York, NY, pp 155–172
Wang B, Liu XZ (2004) Mass production and formulation of nematode-antagonistic microbes. In: Liu XZ, Zhang KQ, Li TF (eds) Biological control of plant-parasitic nematodes (in Chinese, with English abstract). China Science and Technology Press, Beijing, P.R.China, pp 285–297
Wang K-H, Sipes BS, Schnitt DP (2001) Suppression of Rotylenchulus reniformis by Crotalaria juncea, Brassica napus, and Tagetes erecta. Nematropica 31:237–251
Wang K-H, Sipes BS, Schmitt DP (2003) Intercropping cover crops with pineapple for the management of Rotylenchulus reniformis. J Nematol 35:39–47
Wang LF, Yang BJ, Li CD (1999) Evaluation of pathogenicity of parasitic fungi to root-knot nematodes (in Chinese, with English abstract). Sci Silvae Sin 35:41–47
Watson AG, Ford EJ (1972) Soil fungistasis—a reappraisal. Annu Rev Phytopathol 10:327–346
West CP, Izekor E, Oosterhuis DM, Robbins R (1988) The effect of Acremonium coenophialum on the growth and nematode infestation of tall fescue. Plant Soil 112:3–6
Woodward JE, Walker NR, Dillwith JW, Zhang HL, Martin DL (2005) The influence of fungicides on Arthrobotrys oligospora in simulated putting green soil. Ann Appl Biol 146:115–121
Xing LJ, Chen DL, Liu WZ, Duan YX (2002) Influence of some ions on biocontrol system of soybean cyst nematode (in Chinese, with English abstract). Chinese J Biol Control 18:1–5
Yin B, Valinsky L, Gao XB, Becker JO, Borneman J (2003) Bacterial rRNA genes associated with soil suppressiveness against the plant-parasitic nematode Heterodera schachtii. Appl Environ Microbiol 69:1573–1580
Zhou W, Mo MH (2002) Soil fungistasis on the spore germination of fungi (in Chinese, with English abstract). J Yunnan Univ (Nat Sci Edn) 24:312–315
Zhu ML, Zhang KQ, Li TF, Xia ZY, Yang SJ (2001) Study of microorganic nematicide for controlling tobacco knot nematodiasis (in Chinese, with English abstract). J Mt Agric Biol 20:28–31
Zuckerman BM, Dicklow MB, Coles GC, Marban-Mendoza N (1989) Loss of virulence of the endoparasitic fungus Drechmeria coniospora in culture. J Nematol 21:135–137
Acknowledgements
The authors gratefully acknowledge the financial support from the Department of Science and␣Technology of Yunnan Province, P.R.China (No. 2005NG03 and No. 2005NG05).
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Glossary
- Allelopathy
-
a beneficial or detrimental effect from a donor plant to the recipient by chemical pathway (Rice 1984)
- Antagonist
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an umbrella term for parasites, predators, pathogens, competitors, and other organisms that repel, inhibit, or kill plant parasitic nematodes (Sikora 1992)
- Biological control
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the action of parasites, predators or pathogens in maintaining another organism’s population density at a lower average than would occur in their absence (Jatala 1986)
- Biological control of phytonematode
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the reduction in nematode damage by organisms antagonistic towards nematodes through the regulation of nematode populations and/or a reduction in the capacity of nematodes to cause damage, which occurs naturally and is accomplished through the manipulation of environment or by the mass introduction of the antagonist (Sayre and Walter 1991)
- Chemical nematicides
-
the synthetic, not naturally occurring nematicides
- Egg-and female-parasitic fungi
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those nematophagous fungi capable of parasitising the eggs and females, the sedentary stages in the life cycle of nematode
- Endoparasitic fungi
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those nematophagous fungi that do not form trapping organs, but use their spores to infect the nematode hosts
- Endophytic fungi
-
endosymbiotic fungi within plant tissues
- Mycorrhizal fungi
-
mycorrhiza is used to describe the symbiotic association between plant roots and fungi; the fungus receives carbohydrates from the plant and in return supplies the plant with nutrients (especially phosphorus) and hormones (Ryan and Jones 2004)
- Nematode-suppressive soil
-
soils in which phytonematodes cannot establish, soils in which they are found but do not cause disease, or soils in which they cause diseases that subsequently diminish with continuous culture of crops (Yin et al. 2003)
- Nematode-trapping fungi
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those nematophagous fungi with the capacity to capture motile nematodes with specialised trapping organs along the vegetative hyphae
- Nematophagous fungi
-
those fungi with the capacity to capture, parasitise or paralyze nematodes at all stages of their life cycles; they are divided into groups depending on their mode of infection: nematode-trapping, endoparasitic, egg- and female-parasitic, and toxin-producing fungi (Jansson et al. 1997)
- Rhizobia
-
bacteria that display symbiotic interactions with specific legume hosts and nodulate plant roots; rhizobial 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 (Siddiqui and Mahmood 1995)
- Rhizosphere
-
the soil immediately around the root
- Toxin-producing fungi
-
those nematophagous fungi capable of producing nematicidal or nematistatic compounds
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Dong, L.Q., Zhang, K.Q. Microbial control of plant-parasitic nematodes: a five-party interaction. Plant Soil 288, 31–45 (2006). https://doi.org/10.1007/s11104-006-9009-3
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DOI: https://doi.org/10.1007/s11104-006-9009-3