Trichoderma as a Biological Control Agent

Part of the Progress in Biological Control book series (PIBC, volume 11)


Trichoderma species are free-living fungi that are common in soil and root ecosystems. Some strains establish root colonization and enhance growth and development, crop productivity, resistance to abiotic stresses and uptake and use of nutrients. Trichoderma species can antagonize and control a wide range of economically important plant pathogenic fungi, viruses, bacteria and nematodes. Root-knot nematodes, Meloidogyne spp., are sedentary, obligatory root endoparasites of great economic importance, and polyphagous species, such as M. javanica and M. incognita are among the major limiting factors of crops production worldwide. Therefore, these nematodes have been the main target for nematode biocontrol by Trichoderma. Several Trichoderma species and isolates have been evaluated as biocontrol agents against the nematodes with various crops and experimental conditions. Significant results of nematode control and plants growth were achieved. Aiming to improve the biocontrol process, modes of action of the fungus against the root-knot nematodes have been investigated and are described in this chapter. Mechanisms such as parasitism, enzymatic lysis, antibiosis and induced resistance were studied. Understanding the fungus-nematode-plant interactions and the mechanisms of the biocontrol process might contribute to improve the implementation of this biocontrol agent.


Biocontrol Agent Trichoderma Species Nylon Fiber Chitinolytic Enzyme Nematicidal Activity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



culture filtrate


gelatinous matrix


green fluorescent protein


second-stage juvenile


monoclonal antibody


polyclonal antibody


root-knot nematode


surface coat


  1. Alfano G, Lewis Ivey ML, Cakir C et al (2007) Systemic modulation of gene expression in tomato by Trichoderma hamatum 382. Phytopathology 97:429–437PubMedCrossRefGoogle Scholar
  2. Blaxter ML, Robertson WM (1998) The cuticle. In: Perry RN, Wright DJ (eds) Free-living and plant-parasitic nematodes. CAB International, WallingfordGoogle Scholar
  3. Brunner K, Peterbauer CK, Mach RL et al (2003) The Nag1 N-acetylglucosaminidase of Trichoderma atroviride is essential for chitinase induction by chitin and of major relevance to biocontrol. Curr Genet 43:289–295PubMedCrossRefGoogle Scholar
  4. Carsolio C, Benhamou N, Haran S et al (1999) Role of the Trichoderma harzianum endochitinase gene, ech42, in mycoparasitism. Appl Environ Microbiol 65:929–935PubMedGoogle Scholar
  5. Chen S, Dickson DW (2004) Biological control of nematodes by fungal antagonists. In: Chen ZX, Chen SY, Dickson DW (eds) Nematology – advances and prospectives, vol II, Nematode management and utilization. CABI Publishing, CambridgeGoogle Scholar
  6. Cooper WR, Jia L, Goggin L (2005) Effects of jasmonate-induced defences on root-knot nematode infection of resistant and susceptible tomato cultivars. J Chem Ecol 31:1953–1967PubMedCrossRefGoogle Scholar
  7. Cortes C, Gutierrez A, Olmedo V et al (1998) The expression of genes involved in parasitism by Trichoderma harzianum is triggered by a diffusible factor. Mol Gen Genet 260:218–225PubMedCrossRefGoogle Scholar
  8. Davies K (2005) Interactions between nematodes and microorganisms: bridging ecological and molecular approaches. Adv Appl Microbiol 37:53–78CrossRefGoogle Scholar
  9. De Marco JL, Lima LHC, valle de Sousa M et al (2000) A Trichoderma harzianum chitinase destroys the cell wall of the phytopathogen Crinipellis perniciosa, the casual agent of witches’ broom disease of cocoa. World J Microbiol Biotechnol 16:383–386CrossRefGoogle Scholar
  10. Elad Y, Freeman S (2002) Biocontrol of fungal plant pathogens. In: Kempken F (ed) The Mycota, vol XI, Agricultural applications. Springer, Berlin/HeidelbergGoogle Scholar
  11. Elad Y, Barak R, Chet I (1983) Possible role of lectins in mycoparasitism. J Bacteriol 154:1431–1435PubMedGoogle Scholar
  12. Flores A, Chet I, Herrera-Estrella A (1997) Improved biocontrol activity of Trichoderma harzianum by over-expression of the proteinase-encoding gene prb1. Curr Genet 31:30–37PubMedCrossRefGoogle Scholar
  13. Geremia R, Goldman G, Jacobs D et al (1993) Molecular characterization of the proteinase-encoding gene prb1 related to mycoparasitism by Trichoderma harzianum. Mol Microbiol 8:603–613PubMedCrossRefGoogle Scholar
  14. Gravato-Nobre MJ, Evans K (1998) Plant and nematode surfaces: their structure and importance in host-parasite interactions. Nematologica 44:103–124CrossRefGoogle Scholar
  15. Gravato-Nobre MJ, McClure MA, Dolan L et al (1999) Meloidogyne incognita surface antigen epitopes in infected Arabidopsis roots. J Nematol 31:212–223PubMedGoogle Scholar
  16. Haran S, Schickler H, Chet I (1996) Molecular mechanisms of lytic enzymes involved in the biocontrol activity of Trichoderma harzianum. Microbiology 142:2321–2331CrossRefGoogle Scholar
  17. Harman GE (2000) Myths and dogmas of biocontrol. Plant Dis 84:377–391CrossRefGoogle Scholar
  18. Harman GE (2006) Overview of mechanisms and uses of Trichoderma spp. Phytopathology 96:190–194PubMedCrossRefGoogle Scholar
  19. Harman GE, Hayes CK, Lorito M et al (1993) Chitinolytic enzymes of Trichoderma harzianum: purification of chitobiosidase and endochitinase. Phytopathology 83:313–318CrossRefGoogle Scholar
  20. Harman GE, Howell CR, Viterbo A et al (2004) Trichoderma spp. – opportunistic avirulent plant symbionts. Nat Microbiol Rev 2:43–56CrossRefGoogle Scholar
  21. Herrera-Estrella A, Chet I (1998) Biocontrol of bacteria and phytopathogenic fungi. In: Altman A (ed) Agricultural biotechnology. Marcel Dekker, New York/Basel/Hong-KongGoogle Scholar
  22. Howell CR (1998) The role of antibiosis in biocontrol. In: Harman GE, Kubicek CP (eds) Trichoderma and Gliocladium, vol II. Taylor & Francis, PadstowGoogle Scholar
  23. Howell CR (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87:4–10CrossRefGoogle Scholar
  24. Hu GG, McClure MA, Schmitt ME (2000) Origin of a Meloidogyne incognita surface coat antigen. J Nematol 32:174–182PubMedGoogle Scholar
  25. Inbar J, Chet I (1994) A newly isolated lectin from the plant pathogenic fungus Sclerotium rolfsii: purification, characterization, and its role in mycoparasitism. Microbiology 140:651–657PubMedCrossRefGoogle Scholar
  26. Inbar J, Chet I (1997) Lectins in biocontrol. Crit Rev Biotechnol 17:1–20PubMedCrossRefGoogle Scholar
  27. Kerry BR (2000) Rhizosphere interactions and exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annu Rev Phytopathol 38:423–441PubMedCrossRefGoogle Scholar
  28. Kerry BR, Hominick WM (2001) Biological control. In: Lee DL (ed) Biology of nematodes. Taylor & Francis, LondonGoogle Scholar
  29. Khan TA, Saxena SK (1997) Effect of root-dip treatment with fungal filtrates on root penetration, development and reproduction of Meloidogyne javanica on tomato. Int J Nematol 7:85–88Google Scholar
  30. Khan A, Williams KL, Nevalainen HKM (2004) Effects of Pacecilimyces lilacinus protease and chitinase on the eggshell structures and hatching of Meloidogyne javanica juveniles. Biol Control 31:346–352CrossRefGoogle Scholar
  31. Kok CJ, Papert A, Hok-A-Hin CH (2001) Microflora of Meloidogyne egg masses: species composition, population density and effect on the biocontrol agent Verticillium chlamydosporium (Goddard). Nematology 3:729–734CrossRefGoogle Scholar
  32. Koltai H, Sharon E, Spiegel Y (2002) Root-nematode interactions: recognition and pathogenicity. In: Waisel Y, Eshel AA, Kafkafi U (eds) Plant roots: the hidden half, 3rd edn. Marcel Dekker, New YorkGoogle Scholar
  33. Kubicek CP, Mach RL, Peterbauer CK et al (2001) Trichoderma: from genes to biocontrol. J Plant Pathol 83:11–23Google Scholar
  34. Lin H, McClure MA (1996) Surface coat of Meloidogyne incognita. J Nematol 28:216–224PubMedGoogle Scholar
  35. Lopez de Mendoza ME, Curtis R, Gowen S (1999) Identification and characterization of excreted-secreted products and surface coat antigens of animal- and plant-parasitic nematodes. Parasitology 118:397–405PubMedCrossRefGoogle Scholar
  36. Manzanilla-Lopez RH, Kenneth E, Bridge J (2004) Plant diseases caused by nematodes. In: Chen ZX, Chen SY, Dickson DW (eds) Nematology – advances and prospectives, vol II, Nematode management and utilization. CABI Publishing, CambridgeGoogle Scholar
  37. Markovich NA, Kononova GL (2003) Lytic enzymes of Trichoderma and their role in plant defense from fungal diseases: a review. Appl Biochem Microbiol 39:389–400CrossRefGoogle Scholar
  38. Meyer SLF, Massoud SI, Chitwood DJ et al (2000) Evaluation of Trichoderma virens and Burkholderia cepacia for antagonistic activity against root-knot nematode, Meloidogyne incognita. Nematology 2:871–879CrossRefGoogle Scholar
  39. Meyer SLF, Roberts DP, Chitwood DJ et al (2001) Application of Burkholderia cepacia and Trichoderma virens, alone and in combinations, against Meloidogyne incognita on bell pepper. Nematropica 31:75–86Google Scholar
  40. Morton CO, Hirsch PR, Kerry B (2004) Infection of plant-parasitic nematodes by nematophagous fungi – a review of application of molecular biology to understand infection processes and to improve biological control. Nematology 6:161–170CrossRefGoogle Scholar
  41. Oh S-U, Lee S-J, Kim J-H et al (2000) Structural elucidation of new antibiotic peptides, atroviridins A, B and C from Trichoderma atroviridae. Tetrahedron Lett 41:61–64CrossRefGoogle Scholar
  42. Olmedo-Monfil V, Mendoza-Mendoza A, Gómez I et al (2002) Multiple environmental signals determine the transcriptional activation of the mycoparasitism related gene prb1 in Trichoderma atroviridae. Mol Genet Genomics 267:703–712PubMedCrossRefGoogle Scholar
  43. Omero C, Inbar J, Rocha Ramirez V et al (1999) G protein activators and cAMP promote mycoparasitic behavior in Trichoderma harzianum. Mycol Res 103:1637–1642CrossRefGoogle Scholar
  44. Ramot O, Viterbo A, Friesem D et al (2004) Regulation of two homodimer hexosaminidases in the mycoparasitic fungus Trichoderma asperellum by glucosamine. Curr Genet 45:205–213PubMedCrossRefGoogle Scholar
  45. Rao MS, Reddy PP, Nagesh M (1998) Evaluation of plant based formulations of Trichoderma harzianum for the management of Meloidogyne incognita on egg plant. Nematol Medit 26:59–62Google Scholar
  46. Reddy PP, Rao MS, Nagesh M (1996) Management of citrus nematode, Tylenchulus semipenetrans, by integration of Trichoderma harzianum with oil cakes. Nematol Medit 24:265–267Google Scholar
  47. Rocha-Ramirez V, Omero C, Chet I et al (2002) Trichoderma atroviride G-protein α-subunit gene tga1 is involved in mycoparasitic coiling and conidiation Eukar Cell 1:594–605Google Scholar
  48. Saifullah K, Thomas BJ (1996) Studies on the parasitism of Globodera rostochiensis by Trichoderma harzianum using low temperature scanning electron microscopy. Afro-Asian J Nematol 6:117–122Google Scholar
  49. Schickler H, Danin-Gehali B, Haran S (1998) Electrophoretic characterization of chitinases as a tool for the identification of Trichoderma harzianum strains. Mycol Res 102:373–377CrossRefGoogle Scholar
  50. Schirmböck M, Lorito M, Wong Y-L et al (1994) Parallel formation and synergism of hydrolytic enzymes and peptaibol antibiotic action of Trichoderma harzianum against phytopathogenic fungi. Appl Environ Microbiol 60:4364–4370PubMedGoogle Scholar
  51. Sharon E, Spiegel Y (1993) Glycoprotein characterization of the gelatinous matrix in the root-knot nematode Meloidogyne javanica. J Nematol 25:585–589PubMedGoogle Scholar
  52. Sharon E, Spiegel Y (1996) Gold-conjugated reagents for the labelling of carbohydrate-recognition domains and glycoconjugates on nematodes surfaces. J Nematol 28:124–127PubMedGoogle Scholar
  53. Sharon E, Orion D, Spiegel Y (1993) Binding of soil microorganisms and red blood cells by the gelatinous matrix and eggs of Meloidogyne javanica and Rotylenchulus reniformis. Fundam Appl Nematol 16:5–9Google Scholar
  54. Sharon E, Bar-Eyal M, Chet I (2001) Biocontrol of the root-knot nematode Meloidogyne javanica by Trichoderma harzianum. Phytopathology 91:687–693PubMedCrossRefGoogle Scholar
  55. Sharon E, Spiegel Y, Solomon R et al (2002) Characterization of Meloidogyne javanica surface coat using antibodies and their effect on nematode behaviour. Parasitology 125:177–185PubMedCrossRefGoogle Scholar
  56. Sharon E, Chet I, Viterbo A et al (2007) Parasitism of Trichoderma on Meloidogyne javanica and role of the gelatinous matrix. Eur J Plant Pathol 118:247–258CrossRefGoogle Scholar
  57. Sharon E, Chet I, Bar-Eyal M et al (2009a) Biocontrol of root-knot nematodes by Trichoderma – modes of action. Proceedings of IOBC Meeting on Multitrophic Interactions in Soil, Dijon, France. IOBC/WPRS Bulletin 42:159–163Google Scholar
  58. Sharon E, Chet I, Spiegel Y (2009b) Improved attachment and parasitism of Trichoderma on Meloidogyne javanica in vitro. Eur J Plant Pathol 123:291–299Google Scholar
  59. Shoresh M, Yedidia I, Chet I (2005) Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology 95:76–84PubMedCrossRefGoogle Scholar
  60. Sivan A, Chet I (1992) Microbial control of plant diseases. In: Mitchell R (ed) New concepts in environmental microbiology. Wiley-Liss, New YorkGoogle Scholar
  61. Spiegel Y, McClure MA (1995) The surface coat of plant-parasitic nematodes: chemical composition, origin and biological role: a review. J Nematol 27:127–134PubMedGoogle Scholar
  62. Spiegel Y, Inbar J, Kahane I et al (1995) Carbohydrate-recognition domains on the surface of phytophagous nematodes. Exp Parasitol 80:220–227PubMedCrossRefGoogle Scholar
  63. Spiegel Y, Mor M, Sharon E (1996) Attachment of Pasteuria penetrans endospores to the surface of Meloidogyne javanica second-stage juveniles. J Nematol 28:328–334PubMedGoogle Scholar
  64. Spiegel Y, Kahane I, Cohen L et al (1997) Meloidogyne javanica surface proteins: characterization and lability. Parasitology 115:513–519PubMedCrossRefGoogle Scholar
  65. Spiegel Y, Sharon E, Bar-Eyal M (2007) Evaluation and mode of action of Trichoderma isolates as biocontrol agents against plant-parasitic nematodes. IOBC WPRS Bull 30:129–133Google Scholar
  66. St. Leger RJ, Joshi L, Roberts D (1998) Ambient pH is a major determinant in the expression of cuticle-degrading enzymes and hydrophobin by Metarhizium anisopliae. Appl Environ Microbiol 64:709–713Google Scholar
  67. Steyaert JM, Ridgway HJ, Elad Y et al (2003) Genetic basis of mycoparasitism: a mechanism of biological control by species of Trichoderma. N Z J Crop Hort Sci 31:281–291CrossRefGoogle Scholar
  68. Suarez B, Rey M, Castillo P et al (2004) Isolation and characterization of PRA1, a trypsin-like protease from the biocontrol agent Trichoderma harzianum CECT 2413 displaying nematicidal activity. Appl Microbiol Biotechnol 65:46–55PubMedCrossRefGoogle Scholar
  69. Suarez MB, Vizcaino JA, Llobell A (2007) Characterization of genes encoding novel peptidases in the biocontrol fungus Trichoderma harzianum CECT 2413 using the TrichoEST functional genomics approach. Curr Genet 51:331–342PubMedCrossRefGoogle Scholar
  70. Szekeres A, Leitgeb B, Kredics L et al (2005) Peptaibols and related peptaibiotics of Trichoderma: A review. Acta Microbiol Immunol Hung 52:137–168PubMedCrossRefGoogle Scholar
  71. Tikhonov VE, Lopez-Llorca LV, Salinas J et al (2002) Purification and characterization of chitinases from the nematophagous fungi Verticillium chlamydosporium and V Suchlasporium. Fungal Gen Biol 35:67–78CrossRefGoogle Scholar
  72. Trudgill DL, Blok VC (2001) Apomictic, polyphagous root-knot nematodes: exceptionally successful and damaging biotrophic root pathogens. Ann Rev Phytopathol 39:53–77CrossRefGoogle Scholar
  73. Viterbo A, Haran S, Friesem D et al (2001) Antifungal activity of a novel endochitinase gene (chit36) from Trichoderma harzianum Rifai TM. FEMS Microbiol Lett 200:169–174PubMedCrossRefGoogle Scholar
  74. Viterbo A, Montero M, Ramot O et al (2002a) Expression regulation of the endochitinase chit36 from Trichoderma asperellum (T. harzianum T-203). Curr Genet 42:114–122PubMedCrossRefGoogle Scholar
  75. Viterbo A, Ramot O, Chernin L et al (2002b) Significance of lytic enzymes from Trichoderma spp. in the biocontrol of fungal plant pathogens. Antonie Leeuwenhoek 81:549–556PubMedCrossRefGoogle Scholar
  76. Viterbo A, Harel M, Chet I (2004) Isolation of two asparyl proteases from Trichoderma asperellum expressed during colonization of cucumber roots. FEMS Microbiol Lett 238:151–158PubMedGoogle Scholar
  77. Viterbo A, Inbar J, Hadar Y et al (2007a) Plant disease biocontrol and induced resistance via fungal mycoparasites. In: Kubicek CP, Deruzhinina IS (eds) The mycota IV: environmental and microbial relationships, 2nd edn. Springer-Verlag, Berlin/HeidelbergGoogle Scholar
  78. Viterbo A, Wiest A, Brotman Y et al (2007b) The 18mer peptaibols from Trichoderma virens elicit plant defence responses. Mol Plant Pathol 8:737–746PubMedCrossRefGoogle Scholar
  79. Wharton D (1980) Nematode eggshells. Parasitology 81:447–463PubMedCrossRefGoogle Scholar
  80. Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511PubMedGoogle Scholar
  81. Wiest A, Grzegorski D, Xu B-W et al (2002) Identification of peptaibols from Trichoderma virens and cloning of a peptaibol synthetase. J Biol Chem 277:20862–20868PubMedCrossRefGoogle Scholar
  82. Windham GL, Windham MT, Williams WP (1989) Effects of Trichoderma spp. on maize growth and Meloidogyne arenaria reproduction. Plant Dis 73:493–494CrossRefGoogle Scholar
  83. Yedidia I, Benhamou N, Chet I (1999) Induction of defense response in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl Environ Microbiol 65:1061–1070PubMedGoogle Scholar
  84. Yedidia I, Benhamou N, Kapulnik Y et al (2000) Induction and accumulation of PR proteins activity during early stages of root colonization by the mycoparasite T. harzianum strain T-203. Plant Physiol Biochem 38:863–873CrossRefGoogle Scholar
  85. Yedidia I, Srivastva AK, Kapulnik Y et al (2001) Effect of Trichoderma harzianum on microelement concentrations and increased growth of cucumber plants. Plant Soil 235:235–242CrossRefGoogle Scholar
  86. Yedidia I, Shoresh M, Kerem Z et al (2003) Concomitant induction of systemic resistance to Pseudomonas syringae pv. lachrymans in cucumber by Trichoderma asperellum (T-203) and accumulation of phytoalexins. Appl Environ Microbiol 69:7343–7353PubMedCrossRefGoogle Scholar
  87. Zeilinger S, Galhaup C, Payer K et al (1999) Chitinase gene expression during mycoparasitic interaction of Trichoderma harzianum with its host. Fungal Genet Biol 26:131–140PubMedCrossRefGoogle Scholar
  88. Zeilinger S, Reithner B, Scala V et al (2005) Signal transduction by Tga3, a novel G protein α subunit of Trichoderma atroviride. Appl Environ Microbiol 71:1591–1597PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Division of Nematology, Institute of Plant ProtectionARO, The Volcani CenterBet DaganIsrael
  2. 2.Department of Microbiology and Plant Pathology, Faculty of Agricultural, Food and Environmental Quality SciencesHebrew University of JerusalemRehovotIsrael

Personalised recommendations