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CONTROL OF SCLEROTIAL PATHOGENS WITH THE MYCOPARASITE CONIOTHYRIUM MINITANS

  • John M. Whipps
  • Amanda Bennett
  • Mike Challen
  • John Clarkson
  • Emma Coventry
  • S. Muthumeenakshi
  • Ralph Noble
  • Chris Rogers
  • S. Sreenivasaprasad
  • E. Eirian Jones
Conference paper
Part of the NATO Security through Science Series book series

Abstract

Pressure to reduce the use of chemicals in the environment has led to the search for alternative sustainable methods to control soil-borne pathogens, especially those plant pathogens that formlong-lived resting bodies (sclerotia). Mycoparasites that attack sclerotia have been explored as biocontrol agents of these pathogens and some mycoparasites such as Coniothyrium minitans and Trichoderma species have been the focus of particular study. This paper reviews recent developments in the use, ecology, impact and modes of action of C. minitans especially against Sclerotinia sclerotiorum that may be influential in improving reproducibility of disease control in the future. Some studies of the use of Trichoderma viride to control Allium white rot caused by Sclerotium cepivorum are also discussed.

Keywords

Soil Biol Plant Pathol Rhizoctonia Solani Sclerotinia Sclerotiorum Trichoderma Species 
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.

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References

  1. 1.
    J. P. Clarkson, T. Payne, A. Mead, and J. M. Whipps, Selection of fungal biological control agents of Sclerotium cepivorum for control of white rot by sclerotial degradation in a UK soil, Plant Pathol. 51, 735–745 (2002).CrossRefGoogle Scholar
  2. 2.
    P. B. Adams and W. A. Ayers, Ecology of Sclerotinia species, Phytopathology 69, 896–899 (1979).Google Scholar
  3. 3.
    J. R. Coley-Smith, C. M. Mitchell, and C. E. Sansford, Long-term survival of sclerotia of Sclerotium cepivorum and Stromatinia gladioli, Plant Pathol. 39, 58–69 (1990).CrossRefGoogle Scholar
  4. 4.
    G. J. Boland and R. Hall, Index of plant hosts of Sclerotinia sclerotiorum, Can. J. Plant Pathol. 16, 93–108 (1994).CrossRefGoogle Scholar
  5. 5.
    J. M. Whipps, Effects of mycoparasites on sclerotia-forming fungi, in Biotic Interactions and Soil-borne Diseases, edited by A. B. R. Beemster, G. J. Bollen, M. Gerlagh, M. A. Ruissen, B. Schippers, and A. Tempel (Elsevier, Amsterdam, 1991), pp. 129–140.Google Scholar
  6. 6.
    G. E. Harman, C. R. Howell, A. Viterbo, I. Chet, and M. Lorito, Trichoderma species—Opportunistic, avirulent plant symbionts, Nature Rev. Microbiol. 2, 43–56 (2004).CrossRefGoogle Scholar
  7. 7.
    J. M. Whipps and K. G. Davies, Success in biological control of plant pathogens and nematodes by microorganisms, in Biological Control: Measures of Success, edited by G. Gurr and S. Wratten (Kluwer, Dordrecht, 2000), pp. 231–269.Google Scholar
  8. 8.
    APS Biological Control Committee, Commercial products available in the U.S.A. for use against plant pathogens, available at http://www.oardc.ohio-state.edu/apsbcc/ (2006).Google Scholar
  9. 9.
    K. A. El-Tarabily, M. H. Soliman, A. H. Nassar, H. A. Al-Hassani, K. Sivasithamparam, F. McKenna, and G. E. St. J. Hardy, Biological control of Sclerotinia minor using a chitinolytic bacterium and actinomycetes, Plant Pathol. 49, 573–583 (2000).CrossRefGoogle Scholar
  10. 10.
    P. Hebbar, O. Berge, T. Heulin, and S. P. Singh, Bacterial antagonists of sunflower (Helianthus annuus, L) fungal pathogens, Plant Soil 133, 131–140 (1991).CrossRefGoogle Scholar
  11. 11.
    T. J. McLoughlin, J. P. Quinn, A. Bettermann, and R. Bookland, Pseudomonas cepacia suppression of sunflower wilt fungus and role of antifungal compounds in controlling the disease, Appl. Environ. Microbiol. 58, 1760–1763 (1992).PubMedGoogle Scholar
  12. 12.
    C. Thaning, C. J. Welch, J. J. Borowicz, R. Hedman, and B. Gerhardson, Suppression of Sclerotinia sclerotiorum apothecial formation by the soil bacterium Serratia plymuthica: Identification of a chlorinated macrolide as one of the causal agents, Soil Biol. Biochem. 33, 1817–1826 (2001).CrossRefGoogle Scholar
  13. 13.
    J. J. Levenfors, R. Hedman, C. Thaning, B. Gerhardson, and C. J. Welch, Broad-spectrum antifungal metabolites produced by the soil bacterium Serratia plymuthica A 153, Soil Biol. Biochem. 36, 677–685 (2004).CrossRefGoogle Scholar
  14. 14.
    D. J. Hannusch and G. J. Boland, Interactions of air temperature, relative humidity and biological control agents on grey mold of bean, Eur. J. Plant Pathol. 102, 133–142 (1996).CrossRefGoogle Scholar
  15. 15.
    D. J. Hannusch and G. J. Boland, Influence of air temperature and relative humidity on biological control of white mold of bean (Sclerotinia sclerotiorum), Phytopathology 86, 156–162 (1996).CrossRefGoogle Scholar
  16. 16.
    H. C. Huang, E. G. Kokko, L. J. Yanke, and R. C. Phillippe, Bacterial suppression of basal pod rot and end rot of dry peas caused by Sclerotinia sclerotiorum, Can. J. Microbiol. 39, 227–233 (1993).CrossRefGoogle Scholar
  17. 17.
    M. Kamensky, M. Ovadis, I. Chet, and L. Chernin, Soil-borne strain IC14 of Serratia plymuthica with multiple mechanisms of antifungal activity provides biocontrol of Botrytis cinerea and Sclerotinia sclerotiorum diseases, Soil Biol. Biochem. 35, 323–331 (2003).CrossRefGoogle Scholar
  18. 18.
    G. Q. Li, H. C. Huang, and S. N. Acharya, Antagonism and biocontrol potential of Ulocladium atrum on Sclerotinia sclerotiorum, Biol. Control 28, 11–18 (2003).CrossRefGoogle Scholar
  19. 19.
    R. D. Reeleder, The use of yeasts for biological control of the plant pathogen Sclerotinia sclerotiorum, Biocontrol 49, 583–594 (2004).CrossRefGoogle Scholar
  20. 20.
    S. Savchuk and W. G. D. Fernando, Effect of timing of application and population dynamics on the degree of biological control of Sclerotinia sclerotiorum by bacterial antagonists, FEMS Microbiol. Ecol. 49, 379–388 (2004).CrossRefPubMedGoogle Scholar
  21. 21.
    J. P. Clarkson and J. M. Whipps, Control of sclerotial pathogens in horticulture. Pesticide Outlook June 2002, 97–101 (2002).Google Scholar
  22. 22.
    J. M. Whipps, Developments in the biological control of soil-borne plant pathogens, Adv. Bot. Res. 26 1–134 (1997).Google Scholar
  23. 23.
    G. J. Turner and H. T. Tribe, Coniothyrium minitans and its parasitism of Sclerotinia species, Trans. Brit. Mycol. Soc. 66, 97–105 (1976).Google Scholar
  24. 24.
    W. A. Campbell, A new species of Coniothyrium parasitic on sclerotia, Mycologia 39, 190–195 (1947).CrossRefGoogle Scholar
  25. 25.
    C. Monaco, Evaluation of the efficiency of mycoparasites on Sclerotinia sclerotiorum “in vitro,” Rev. Fac. Agronomia 65, 67–73 (1989).Google Scholar
  26. 26.
    C. Sandys-Winsch, J. M. Whipps, M. Gerlagh, and M. Kruse, World distribution of the sclerotial mycoparasite Coniothyrium minitans, Mycol. Res. 97, 1175–1178 (1993).Google Scholar
  27. 27.
    S. P. Budge and J. M. Whipps, Glasshouse trials of Coniothyrium minitans and Trichoderma species for the biological control of Sclerotinia sclerotiorum in celery and lettuce, Plant Pathol. 40, 59–66 (1991).CrossRefGoogle Scholar
  28. 28.
    H. C. Huang and J. A. Hoes, Importance of plant spacing and sclerotial position to development of Sclerotinia wilt of sunflower, Plant Dis. 64, 81–84 (1980).CrossRefGoogle Scholar
  29. 29.
    M. Gerlagh, H. M. Goossen-van de Geijn, N. J. Fokkema, and P. F. G. Vereijken, Long-term biosanitation by application of Coniothyrium minitans on Sclerotinia sclerotiorum infected crops, Phytopathology 89, 141–147 (1999).CrossRefPubMedGoogle Scholar
  30. 30.
    P. Lüth, The control of Sclerotinia spp. and Sclerotium cepivorum with the biological fungicide Contans® WG—experiences from field trials and commercial use, in Proceedings of the XI International Sclerotinia Workshop, York, England, July 8–12, 2001, edited by C. S. Young and K. J. D. Hughes (Central Science Laboratory, York, 2001), pp. 37–38.Google Scholar
  31. 31.
    D. L. McLaren, H. C. Huang, G. C. Kozub, and S. R. Rimmer, Biological control of Sclerotinia wilt of sunflower with Talaromyces flavus and Coniothyrium minitans, Plant Dis. 78, 231–235 (1994).CrossRefGoogle Scholar
  32. 32.
    A. H. M. Ahmed and H. T. Tribe, Biological control of white rot of onion (Sclerotium cepivorum) by Coniothyrium minitans, Plant Pathol. 26, 75–78 (1977).CrossRefGoogle Scholar
  33. 33.
    M. P. McQuilken, S. J. Mitchell, S. P. Budge, J. M. Whipps, J. S. Fenlon, and S. A. Archer, Effect of Coniothyrium minitans on sclerotial survival and apothecial production of Sclerotinia sclerotiorum in field-grown oilseed rape, Plant Pathol. 44, 883–896 (1995).CrossRefGoogle Scholar
  34. 34.
    E. E. Jones and J. M. Whipps, Effect of inoculum rates and sources of Coniothyrium minitans on control of Sclerotinia sclerotiorum disease in glasshouse lettuce, Eur. J. Plant Pathol. 108, 527–538 (2002).CrossRefGoogle Scholar
  35. 35.
    H. C. Huang and G. C. Kozub, Monocropping to sunflower and decline of Sclerotinia wilt, Bot. Bull. Acad. Sinica 32, 163–170 (1991).Google Scholar
  36. 36.
    M. Gerlagh, H. M. Goossen-van de Geijn, A. E. Hoogland, and P. F. G. Vereijken, Quantitative aspects of infection of Sclerotinia sclerotiorum sclerotia by Coniothyrium minitans—Timing of application, concentration and quality of conidial suspension of the mycoparasite, Eur. J. Plant Pathol. 109, 489–502 (2003).CrossRefGoogle Scholar
  37. 37.
    M. Gerlagh, H. M. Goossen-van de Geijn, A. E. Hoogland, P. F. G. Vereijken, P. F. M. Horsten, and B. H. de Haas, Effect of volume and concentration of conidial suspensions of Coniothyrium minitans on infection of Sclerotinia sclerotiorum sclerotia, Biocontrol Sci. Technol. 14, 675–690 (2004).CrossRefGoogle Scholar
  38. 38.
    H. C. Huang, E. Bremer, R. K. Hynes, and R. S. Erickson, Foliar application of fungal biocontrol agents for the control of white mold of dry bean caused by Sclerotinia sclerotiorum, Biol. Control 18, 270–276 (2000).CrossRefGoogle Scholar
  39. 39.
    G. Q. Li, H. C. Huang, and S. N. Acharya, Importance of pollen and senescent petals in the suppression of alfalfa blossom blight (Sclerotinia sclerotiorum) by Coniothyrium minitans, Biocontrol Sci. Technol. 13, 495–505 (2003).CrossRefGoogle Scholar
  40. 40.
    P. Trutmann, P. J. Keane, and P. R. Merriman, Biological control of Sclerotinia sclerotiorum on aerial parts of plants by the hyperparasite Coniothyrium minitans, Trans. Brit. Mycol. Soc. 78, 521–529 (1982).Google Scholar
  41. 41.
    S. P. Budge, M. P. McQuilken, J. S. Fenlon, and J. M. Whipps, Use of Coniothyrium minitans and Gliocladium virens for biological control of Sclerotinia sclerotiorum in glasshouse lettuce, Biol. Control 5, 513–522 (1995).CrossRefGoogle Scholar
  42. 42.
    M. P. McQuilken, S. P. Budge, and J. M. Whipps, Production, survival and evaluation of liquid culture-produced inocula of Coniothyrium minitans against Sclerotinia sclerotiorum, Biocontrol Sci. Technol. 7, 23–36 (1997).CrossRefGoogle Scholar
  43. 43.
    T. de Vrije, N. Antoine, R. M. Buitelaar, S. Bruckner, M. Dissevelt, A. Durand, M. Gerlagh, E. E. Jones, P. Lüth, J. Oostra, W. J. Ravensberg, R. Renaud, A. Rinzema, F. J. Weber, and J. M. Whipps, The fungal biocontrol agent Coniothyrium minitans: production by solid-state fermentation, application and marketing, Appl. Microbiol. Biotechnol. 56, 58–68 (2001).PubMedCrossRefGoogle Scholar
  44. 44.
    E. E. Jones, A. Mead, and J. M. Whipps, Evaluation of different Coniothyrium minitans inoculum sources and application rates on apothecial production and infection of Sclerotinia sclerotiorum sclerotia, Soil Biol. Biochem. 35, 409–419 (2003).CrossRefGoogle Scholar
  45. 45.
    E. E. Jones and A. Stewart, Selection of mycoparasites of sclerotia of Sclerotinia sclerotiorum isolated from New Zealand soils, N. Z. J. Crop Hort. Sci. 28, 105–114 (2000).Google Scholar
  46. 46.
    E. E. Jones, A. Mead, and J. M. Whipps, Effect of inoculum type and timing of application of Coniothyrium minitans on Sclerotinia sclerotiorum: control of sclerotinia disease in glasshouse lettuce. Plant Pathol. 53, 611–620 (2004).CrossRefGoogle Scholar
  47. 47.
    E. E. Jones, J. P. Clarkson, A. Mead, and J. M. Whipps, Effect of inoculum type and timing of application of Coniothyrium minitans on Sclerotinia sclerotiorum: Influence on apothecial production, Plant Pathol. 53, 621–628 (2004).CrossRefGoogle Scholar
  48. 48.
    M. P. McQuilken, S. P. Budge, and J. M. Whipps, Effects of culture media and environmental factors on conidial germination, pycnidial production and hyphal extension of Coniothyrium minitans, Mycol. Res. 101, 11–17 (1997).CrossRefGoogle Scholar
  49. 49.
    E. E. Jones, A. Stewart, and J. M. Whipps, Use of Coniothyrium minitans transformed with the hygromycin B resistance gene to study survival and infection of Sclerotinia sclerotiorum sclerotia in soil, Mycol. Res. 107, 267–276 (2003).PubMedCrossRefGoogle Scholar
  50. 50.
    J. M. Whipps, Microbial interactions and biocontrol in the rhizosphere, J. Exp. Bot. 52, 487–511 (2001).PubMedGoogle Scholar
  51. 51.
    R. Noble and E. Coventry, Suppression of soil-borne plant diseases with composts: A review, Biocontrol Sci. Technol. 15, 3–20 (2005).CrossRefGoogle Scholar
  52. 52.
    M. C. A. van Loenen, Y. Turbett, C. E. Mullins, N. E. H. Feilden, M. J. Wilson, C. Leifert, and W. E. Seel, Low temperature-short duration steaming of soil kills soil-borne pathogens, nematode pests and weeds, Eur. J. Plant Pathol. 109, 993–1002 (2003).CrossRefGoogle Scholar
  53. 53.
    S. P. Budge and J. M. Whipps, Potential for integrated control of Sclerotinia sclerotiorum in glasshouse lettuce using Coniothyrium minitans and reduced fungicide application, Phytopathology 91, 221–227 (2001).CrossRefPubMedGoogle Scholar
  54. 54.
    A. J. Bennett, C. Leifert, and J. M. Whipps, Effect of combined treatment of pasteurisation and Coniothyrium minitans on sclerotia of Sclerotinia sclerotiorum in soil, Eur. J. Plant Pathol. 113, 197–209 (2005).CrossRefGoogle Scholar
  55. 55.
    R. H. Williams, J. M. Whipps, and R. C. Cooke, Role of soil mesofauna in dispersal of Coniothyrium minitans: Transmission to sclerotia of Sclerotinia sclerotiorum, Soil Biol. Biochem. 30, 1929–1935 (1998).CrossRefGoogle Scholar
  56. 56.
    R. H. Williams, J. M. Whipps, and R. C. Cooke, Role of soil mesofauna in dispersal of Coniothyrium minitans: Mechanisms of transmission, Soil Biol. Biochem. 30, 1937–1945 (1998).CrossRefGoogle Scholar
  57. 57.
    P. Trutmann, P. J. Keane, and P. R. Merriman, Reduction of sclerotial inoculum of Sclerotinia sclerotiorum with Coniothyrium minitans, Soil Biol. Biochem. 12, 461–465 (1980).CrossRefGoogle Scholar
  58. 58.
    J. M. Whipps, Growth of the collembolan Folsomia candida on cultures of the mycoparasite Coniothyrium minitans and sclerotia of Sclerotinia sclerotiorum, Mycol. Res. 97, 1277–1280 (1993).Google Scholar
  59. 59.
    J. M. Whipps and S. P. Budge, Transmission of the mycoparasite Coniothyrium minitans by collembolan Folsomia candida (Collembola, Entomobryidae) and glasshouse sciarid-Bradysia sp. (Diptera, Sciaridae), Ann. Appl. Biol. 123, 165–171 (1993).CrossRefGoogle Scholar
  60. 60.
    S. J. Kay and A. Stewart, Evaluation of fungal antagonists for control of onion white-rot in soil box trials, Plant Pathol. 43, 371–377 (1994).CrossRefGoogle Scholar
  61. 61.
    J. P. Clarkson, A. Scruby, A. Mead, C. Wright, B. Smith, and J. M. Whipps, Integrated control of Allium white rot with Trichoderma viride, tebuconazole and composted onion waste, Plant Pathol. 55, 375–386 (2006).CrossRefGoogle Scholar
  62. 62.
    E. Coventry, R. Noble, A. Mead, and J. M. Whipps, Control of Allium white rot (Sclerotium cepivorum) with composted onion waste, Soil Biol. Biochem. 34, 1037–1045 (2002).CrossRefGoogle Scholar
  63. 63.
    E. Coventry, R. Noble, A. Mead, and J. M. Whipps, Suppression of Allium white rot (Sclerotium cepivorum) in different soils using vegetable wastes, Eur. J. Plant Pathol. 111, 101–112 (2005).CrossRefGoogle Scholar
  64. 64.
    E. Coventry, R. Noble, A. Mead, F. R. Marin, J. A. Perez, and J. M. Whipps, Allium white rot suppression with composts and Trichoderma viride in relation to sclerotia viability, Phytopathology 96, 1009–1020 (2006).CrossRefPubMedGoogle Scholar
  65. 65.
    J. P. Clarkson, A. Mead, T. Payne, and J. M. Whipps, Effect of environmental factors and Sclerotium cepivorum isolate on sclerotial degradation and biological control of white rot by Trichoderma, Plant Pathol. 53, 353–362 (2004).CrossRefGoogle Scholar
  66. 66.
    Y. Ramona and M. A. Line, Potential for the large-scale production of a biocontrol fungus—In raw and composted paper mill waste, Compost Sci. Utiliz. 10, 57–62 (2002).Google Scholar
  67. 67.
    J. M. Whipps and M. Gerlagh, Biology of Coniothyrium minitans and its potential for use in disease biocontrol, Mycol. Res. 96, 897–907 (1992).CrossRefGoogle Scholar
  68. 68.
    J. M. Whipps, Ecological and biotechnological considerations in enhancing disease biocontrol, in Enhancing Biocontrol Agents and Handling Risks, edited by M. Vurro, J. Gressel, T. Butt, G. E. Harman, A. Pilgeram, R. J. St. Leger, D. L. Nuss (IOS Press, Ohmsha, 2001), pp. 43–51.Google Scholar
  69. 69.
    H. C. Huang, Distribution of Coniothyrium minitans in Manitoba sunflower fields, Can. J. Plant Pathol. 3, 219–222 (1981).CrossRefGoogle Scholar
  70. 70.
    E. E. Jones, M. Carpenter, D. Fong, A. Goldstein, A. Thrush, A. Crowhurst, and A. Stewart, Co-transformation of the sclerotial mycoparasite Coniothyrium minitans with hygromycin B resistance and β-glucuronidase markers, Mycol. Res. 103, 929–937 (1999).CrossRefGoogle Scholar
  71. 71.
    R. H. Williams, Dispersal of the mycoparasite Coniothyrium minitans, PhD thesis (Department of Animal and Plant Sciences, University of Sheffield, Sheffield, 1996), p. 144.Google Scholar
  72. 72.
    M. J. Butler and A. W. Day, Fungal melanins: A review, Can. J. Microbiol. 44, 1115–1136 (1998).CrossRefGoogle Scholar
  73. 73.
    H. T. Tribe, On the parasitism of Sclerotinia trifoliorum by Coniothyrium minitans, Trans. Brit. Mycol. Soc. 40, 489–499 (1957).CrossRefGoogle Scholar
  74. 74.
    A. J. Bennett, C. Leifert, and J. M. Whipps, Survival of Coniothyrium minitans associated with sclerotia of Sclerotinia sclerotiorum in soil, Soil Biol. Biochem. 38, 164–172 (2006).CrossRefGoogle Scholar
  75. 75.
    T. A. Brimner and G. J. Boland, A review of the non-target effects of fungi used to biologically control plant diseases, Agr. Ecosyst. Environ.100, 3–16 (2003).CrossRefGoogle Scholar
  76. 76.
    A. Winding, S. J. Binnerup, and H. Pritchard, Non-target effects of bacterial biological control agents suppressing root pathogenic fungi, FEMS Microbiol. Ecol. 47, 129–141 (2004).CrossRefPubMedGoogle Scholar
  77. 77.
    M. P. McQuilken, J. Gemmell, and J. M. Whipps, Some nutritional factors affecting production of biomass and antifungal metabolites of Coniothyrium minitans, Biocontrol Sci. Technol. 12, 443–454 (2002).CrossRefGoogle Scholar
  78. 78.
    M. P. McQuilken, J. Gemmell, R. A. Hill, and J. M. Whipps, Production of macrosphelide A by the mycoparasite Coniothyrium minitans, FEMS Microbiol. Lett. 219, 27–31 (2003).PubMedCrossRefGoogle Scholar
  79. 79.
    M. Li, X. Gong, J. Zheng, D. Jiang, Y. Fu, and M. Hou, Transformation of Coniothyrium minitans, a parasite of Sclerotinia sclerotiorum, with Agrobacterium tumefaciens, FEMS Microbiol. Lett. 243, 323–329 (2005).PubMedCrossRefGoogle Scholar
  80. 80.
    A. J. Bennett, C. Leifert, and J. M. Whipps, Survival of the biocontrol agents Coniothyrium minitans and Bacillus subtilis MBI 600 introduced into pasteurised, sterilised and non-sterile soils, Soil Biol. Biochem. 35, 1565–1573 (2003).CrossRefGoogle Scholar
  81. 81.
    P. Garbeva, J. A. van Veen, and J. D. van Elsas, Microbial diversity in soil: Selection of microbial populations by plant and soil type and implications for disease suppressiveness, Annu. Rev. Phytopathol. 42, 243–270 (2004).PubMedCrossRefGoogle Scholar
  82. 82.
    M. Mazzola, Assessment and management of soil microbial community structure for disease suppression, Annu. Rev. Phytopathol. 42, 35–59 (2004).PubMedCrossRefGoogle Scholar
  83. 83.
    P. J. Hunter, G. M. Petch, A. A. Calvo-Bado, T. R. Pettitt, N. Parsons, J. A. W. Morgan, and J. M. Whipps, Microbial characteristics of peats associated with suppression of damping-off disease caused by Pythium sylvaticum, Appl. Environ. Microbiol. 72, 6452–6460 (2006).PubMedCrossRefGoogle Scholar
  84. 84.
    A. Mendoza-Mendoza, M. J. Pozo, D. Grzegorski, P. Martínez, J. M. García, V. Olmedo-Monfil, C. Cortés, C. Kenerley, and A. Herrera-Estrella, Enhanced biocontrol activity of Trichoderma through inactivation of a mitogen-activated protein kinase, Proc. Natl. Acad. Sci. USA 100, 15965–15970 (2003).PubMedCrossRefGoogle Scholar
  85. 85.
    J. M. Steyaert, H. J. Ridgway, Y. Elad, and A. Stewart, Genetic basis of mycoparasitism: a mechanism of biological control by species of Trichoderma, N. Z. J. Crop Hort. Sci. 31, 281–291 (2003).Google Scholar
  86. 86.
    J. M. Steyaert, A. Stewart, M. Jaspers, M. Carpenter, and H. J. Ridgway, Co-expression of two genes, a chitinase (chit42) and proteinase (prb1), implicated in mycoparasitism by Trichoderma hamatum, Mycologia 96, 1245–1252 (2004).Google Scholar
  87. 87.
    P. K. Mukherjee, J. Latha, R. Hadar, and B. A. Horwitz, Role of two G-protein alpha subunits, TgaA and TgaB, in the antagonism of plant pathogens by Trichoderma virens, Appl. Environ. Microbiol. 70, 542–549 (2004).PubMedCrossRefGoogle Scholar
  88. 88.
    M. A. Carpenter, A. Stewart, and H. J. Ridgway, Identification of novel Trichoderma hamatum genes expressed during mycoparasitism using subtractive hybridization, FEMS Microbiol. Lett. 251, 105–112 (2005).PubMedCrossRefGoogle Scholar
  89. 89.
    P. G. Liu and Q. Yang, Identification of genes with a biocontrol function in Trichoderma harzianum mycelium using the expressed sequence tag approach, Res. Microbiol. 156, 416–423 (2005).PubMedCrossRefGoogle Scholar
  90. 90.
    Trichoest, available at www.trichoderma.org (2006).Google Scholar
  91. 91.
    Broad Institute, available at www.broad.mit.edu/annotation/fungi/sclerotinia_sclerotiorum (2006).Google Scholar
  92. 92.
    C. W. Rogers, M. P. Challen, J. R. Green, and J. M. Whipps, Use of REMI and Agrobacterium-mediated transformation to identify pathogenicity mutants of the biocontrol fungus, Coniothyrium minitans, FEMS Microbiol. Lett. 241, 207–214 (2004).PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • John M. Whipps
    • 1
  • Amanda Bennett
    • 1
  • Mike Challen
    • 1
  • John Clarkson
    • 1
  • Emma Coventry
    • 1
  • S. Muthumeenakshi
    • 1
  • Ralph Noble
    • 1
  • Chris Rogers
    • 1
  • S. Sreenivasaprasad
    • 1
  • E. Eirian Jones
    • 2
  1. 1.Warwick HRIUniversity of WarwickWarwickUK
  2. 2.National Centre for Advanced Bio-Protection TechnologiesLincoln UniversityCanterburyNew Zealand

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