Beneficial and Harmful Aspects of Trichoderma : A Review

Authors

  • Priya Solanki  C. G. Bhakta Institute of Biotechnology, Uka Tarsadia University, Gopal vidya nagar, Tarsadi, Bardoli-Mahuva road, Surat (dist), Gujarat, India
  • Srivathsa Nallanchakravarthula  C. G. Bhakta Institute of Biotechnology, Uka Tarsadia University, Gopal vidya nagar, Tarsadi, Bardoli-Mahuva road, Surat (dist), Gujarat, India

Keywords:

Trichoderma, Biocontrol, Myco-Parasitism, Biofertilizer, Rhizosphere

Abstract

Microorganisms or their metabolites are being employed for the plant health and nutrient acquisition. Trichoderma species is one such fungal organism that is recognised for its biocontrol potential against various plant pathogens especially in rhizosphere. Their ability to protect in wide soil environments and mechanisms are widely studied. It is known to have various strategies and potential metabolites that influence plant and the pathogens, such as mycoparasitism and induced resistance. Not only beneficial but Trichoderma is also known to have some harmful effects. This review focuses on the both the beneficial and harmful aspects of Trichoderma for the environment and as well as some of its molecular aspects during its interactions.

References

  1. Persoon, C. H. 1794. Neuer Veersu cheinersy stematischen Eintheilung der Schwamme (Dispositiomethodicafungorum). Romer’s News Mag. Bot. 1:63-128
  2. Weindling, R. 1934. Studies on a lethal principle effective in the parasitic action of Trichoderma lignorum on Rhizoctonia solani and other soil fungi. Phytopathology 24:1153-1179.
  3. Weindling, R., and Fawcett, H. S. 1936. Experiments in the control of Rhizoctonia damping-off of citrus seedlings. J. Agric. Sci. Calif. Agric. Exp. Stn. 10:1-16.
  4. R?czey,K., Szengyel,Z., Eklund,R., Zacchi,G. 1996. Cellulase production by T. reesei. BioresourceTechnol 57: 25-30.
  5. Juh?sz,T., Kozma,K., Szengyel,Z., R?czey,K. 2003. Production of ?-glucosidase by mixed culture of Aspergillus niger BKMF 1305 and Trichoderma reesei RUT C30. Food Technol Biotechnol. 41: 49-53.
  6. Brewer, D., Calder, F.W., Macintyre, T.M. and Taylor, A. 1971. Ovine ill-thrift in Nova Scotia: The possible regulation of the ruman flora in sheep by the fungal flora of permanent pasture. J. Agric. Sci.76:465-477.
  7. Danielson, R.M. and Davey, C.B. 1973. The abundance of Trichoderma propagules and the distribution of species in forest soils. Soil Biol. Biochem. 5:485-494.
  8. Domsch, K.H.; Gams, W. and Anderson, T.H. 1980. Compendium of Soil fungi. Academic Press, London, pp. 794-809.
  9. Chang, Y.-C., Chang, Y.-C., Baker, R., Kleifeld, O., and Chet, I. 1986. Increased growth of plants in the presence of the biological control agent Trichoderma harzianum. Plant Dis. 70:145-148.
  10. Lindsey, D. L., and Baker, R. 1967. Effect of certain fungi on dwarf tomatoes grown under gnotobiotic conditions. Phytopathology 57:1262-1263.
  11. Chet, I., and Baker, R. 1981. Isolation and biocontrol potential of Trichoderma harzianum from soil naturally suppressive of Rhizoctonia solani. Phytopathology. 71:286-290.
  12. Mandels, M. 1975. Microbial sources of cellulase. Biotechnol. Bioeng. Sym. 5:81-105.
  13. Mandels, M., and Reese, E. T. 1957. Induction of cellulase in Trichoderma virideas influenced by carbon sources and metals. J. Bacteriol. 73:269-278
  14. Elad, Y., Chet, I., and Henis, Y. 1982. Degradation of plant pathogenic fungi by Trichoderma harzianum. Can. J. Microbiol. 28:719-725.
  15. Lorito, M., Woo, S. L., Donzelli, B., and Scala, F. 1996. Synergistic, antifungal interactions of chitinolytic enzymes from fungi, bacteria and plants. Pages 157-164 in: Chitin Enzymology II. R. A. A. Muzzarelli, ed. Atec, Grottammare (AP), Italy.
  16. Sivan,A., Chet, I. 1986. Biological control of Fusarium spp. in cotton, wheat and muskmelon by Trichoderma harzianum. J Phytopathol 116. 39-47.
  17. Na?r,Z., Kecsk?s,M. 1995. A method for selecting Trichoderma strains antagonistic against Sclerotinia minor. Microbiol Res 150, 239-246.
  18. Naseby,D.C., Pascual,J.A., Lynch,J.M. 2000. Effect of biocontrol strains of Trichoderma on plant growth, Pythium ultimum populations, soil microbial communities and soil enzyme activities. J ApplMicrobiol. 88: 161-169.
  19. Papavizas,G.C. 1985. Trichoderma and Gliocladium: biology, ecology, and potential for biocontrol. Annu Rev Phytopathol. 23: 23-54.
  20. Manczinger,L., Antal,Z., Kredics,L. 2002. Ecophysiology and breeding of mycoparasitic Trichoderma strains. Acta Microbiol Immunol Hung 49: 1-14.
  21. Bigirimana, J., De Meyer, G., Poppe, J., Elad, Y., and Hofte, M. 1997. Induction of systemic resistance on bean (Phaseolus vulgaris) by Trichoderma harzianum. Med. Fac. Landbouww. Univ. Gent 62:1001-1007.
  22. Harman, G. E., Howell, C. R., Viterbo, A., Chet, I., and Lorito, M. 2004. Trichoderma species?Opportunistic, avirulent plant symbionts. Nat. Rev. Microbiol. 2:43-56.
  23. Yedidia, I., Benhamou, N., and Chet, I. 1999. Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl. Environ. Microbiol. 653:1061-1070.
  24. Hwang, J., and Benson, D. M. 2003. Expression of induced resistance in poinsettia cuttings against Rhizoctonia stem rot by treatment of stock plants with binucleate Rhizoctonia. Biol. Control. 27:73-80.
  25. Benhamou, N., Garand, C., and Goulet, A. 2002. Ability of nonpathogenic Fusarium oxysporum strain Fo47 to induce resistance against Pythium ultimum infection in cucumber. Appl. Environ. Microbiol. 68:4044-4060.
  26. Monte E (2001) Understanding Trichoderma: between biotechnology and microbial ecology. IntMicrobiol. 4:1-4
  27. Grondona I, Hermosa R, Tejada M, Gomis MD, Mateos PF, Bridge PD, Monte E, Garc?a-Acha I. 1997. Physiological and biochemical characterization of Trichoderma harzianum, a biological control agent against soil-borne fungal plant pathogens. Appl Environ Microbiol 63:3189-3198
  28. Chet I, Inbar J, Hadar I .1997. Fungal antagonists and mycoparasites. In: Wicklow DT, S?derstr?m B (eds) The Mycota IV: Environmental and microbial relationships. Springer-Verlag, Berlin, pp 165-184.
  29. Foreyt,W.J., Leathers,C.W. 1985. Trichoderma spp. infection in the alligator (Alligator mississippiensis). J Herpetol. 19: 530-531.
  30. Jacobson,E.R. 1980. Necrotizing mycotic dermatitis in snakes: clinical and pathologic features. J Am Vet Med Assoc. 177: 838-841.
  31. Woo SL, Scala F, Ruocco M, Lorito M. 2006. The molecular biology of the interactions between Trichoderma spp.,pathogenic fungi, and plants. Phytopathology 96:181-185.
  32. Lorito M, Woo SL, Harman GE, Monte E. 2010. Translational research on Trichoderma: from omics to the field. Annu Rev Phytopathol. 48:395-417.
  33. Vinale F, Marra R, Scala F, Ghisalberti EL, Lorito M, Sivasithamparam K. 2006. Major secondary metabolites produced by two commercial Trichoderma strains active against different phytopathogens. Lett. Appl. Microbiol. 43:143-148
  34. Verma M, Brar SK, Tyagi RD, Surampalli RY, Valero JR. 2007. Antagonistic fungi, Trichoderma spp.: Panoply of biological control. Biochem. Eng. J. 37:1-20.
  35. Sarrocco S, Guidi L, Fambrini S, Del’Innocenti E, Vannacci G. 2009. Competition for cellulose exploitation between Rhizoctonia solani and two Trichoderma isolates in the decomposition of wheat straw. J. Plant Pathol. 91:331-338.
  36. Alabouvette C, Olivain C, Migheli Q, Steinberg C. 2009. Microbiological control of soil-borne phytopathogenic fungi with special emphasis on wilt-inducing Fusarium oxysporum. New. Phytol. 184:529-544.
  37. Tjamos EC, Papavizas GC, Cook RJ. 1922. In: Biological control of plant diseases. Progress and challenges for the future. Plenum Press, New York. P 222.
  38. Chet I, Inbar J. 1994.Biological control of fungal pathogens. Appl. Biochem. Biotechnol. 48:37-43.
  39. Latorre BA, Lillo C, Rioja ME. 2001. Eficacia de los tratamientos fungicidas para el control de Botrytis cinerea de la vid en funci?n de la ?poca de aplicaci?n. Cienc. Inv. Agric. 28:61-66.
  40. Rahman MA, Begum MF, Alam MF. 2009 . Screening of Trichoderma isolates as a biological control agent against Ceratocystis paradoxa causing pineapple disease of Sugarcane. Mycobiology 37:277-285.
  41. Saloheimo M, Paloheimo M, Hakola S, Pere J, Swanson B, Nyyss?nen E, Bhatia A, Ward M, Swollenin MP. 2002. A Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials. Eur. J. Biochem. 269:4202-4211.
  42. Viterbo A, Harel M, Chet I (2004). Isolation of two aspartyl proteases from Trichoderma asperellum expressed during colonization of cucumber roots. FEMS Microbiol. Lett. 238:151-158.
  43. Brotman Y, Briff E, Viterbo A, Chet I .2008. Role of swollenin, an expansin-like protein from Trichoderma, in plant root colonization. Plant Physiol. 147:779-789.
  44. Samolski I, Rinc?n AM, Pinz?n LM, Viterbo A, Monte E. 2012. The qid74 gene from Trichoderma harzianum has a role in root architecture and plant biofertilization. Microbiology 158:129-138.
  45. Ben?tez T, Rinc?n AM, Lim?n MC, Cod?n AC. 2004. Biocontrol mechanisms of Trichoderma strains. Int. Microbiol. 7: 249-260.
  46. Cumagun CJR, Ilag LL. 1997. Enhancing the Efficacy of Trichoderma harzianum Rifai by Chitin amendment against sheath blight of rice. Phil. Phytopathol. 33:72-86.
  47. Howell CR. 1998. The role of antibiosis in biocontrol. In: Trichoderma & Gliocladium. Harman GE, Kubicek CP (Eds.). 2. Taylor & Francis, Padstow. pp. 173-184.
  48. Rey M, Delgado-Jarana J, Ben?tez T. 2001. Improved antifungal activity of a mutant of Trichoderma harzianum CECT 2413 which produces more extracellular proteins. Appl. Microbiol. Biotechnol. 55:604-608.
  49. Wiest A, Grzegorski D, Xu B. 2002. Identification of peptaibols from Trichoderma virens and cloning of a peptaibol synthetase. J. Biol. Chem. 277:20862-20868.
  50. Vey A, Hoagland RE, Butt TM. 2001. Toxic metabolites of fungal biocontrol agents. In: Fungi as biocontrol agents: Progress, problems and potential. Butt TM, Jackson C, Magan N (Eds.). CABI, Bristol, UK, pp. 311-346.
  51. Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Mo?nne-Loccoz Y. 2009. The rhizosphere: a playground and battle-field for soil-borne pathogens and beneficial microorganisms. Plant Soil. 321:341-361.
  52. Daguerre Y, Siegel K, Edel-Hermann V, Steinberg C. 2014. Fungal proteins and genes associated with biocontrol mechanisms of soil-borne pathogens: a review. Fungal Biol Rev. 28:97-125.
  53. Zeilinger S, Galhaup C, Payer K, Woo SL, Mach RL, Fekete C, Lorito M, Kubicek CP. 1999. Chitinase gene expression during mycoparasitic interaction of Trichoderma harzianum with its host. Fungal Genet. Biol. 26:131-140.
  54. Gajera H, Domadiya R, Patel S, Kapopara M, Golakiya B. 2013. Molecular mechanism of Trichoderma as bio-control agents against phytopathogen system - a review. Curr. Res. Microbiol. Biotechnol. 1:133-142.
  55. Howell CR. 2003. Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis. 87:4-10.
  56. Piotrowski M, Volmer JJ. 2006. Cyanide metabolism in higher plants: cyanoalanine hydratase is a NIT4 homolog. Plant. Mol. Biol. 61:111-122.
  57. Gazis R, Chaverri P. 2010. Diversity of fungal endophytes in leaves and stems of rubber trees (Hevea brasiliensis) in Tambopata, Peru. Fungal Ecol. 4:94-102.
  58. Chaverri P, Gazis R, Samuels GJ. 2011. Trichoderma amazonicum, a new endophytic species on Hevea brasiliensis and H. guianensis from the Amazon basin. Mycologia. 103:139-151.
  59. Chaverri P, Samuels GJ. 2013.Evolution of habitat preference and nutrition mode in a cosmopolitan fungal genus with evidence of inter kingdom host jumps and major shifts in ecology. Evolution 67:2823-2837.
  60. Harman GE, Herrera-Estrella AH, Benjamin A, Matteo L. 2012. Special issue: Trichoderma - from Basic Biology to Biotechnology. Microbiology 58:1-2.
  61. Molna?r-Ga?bor E, Do?czi I, Hatvani L, Vagv?lgyi C and Kredics L. 2013. Isolated sinusitis sphenoidalis caused by Trichoderma longibrachiatum in an immunocompetent patient with headache. Journal of Medical Microbiology. 62.1249-1252
  62. Samuels GJ, Dodd S, Lu BS, Petrini O, Schroers HJ, Druzhinina IS. 2006. The Trichoderma koningii aggregate species. Stud. Mycol. 56:67-133.
  63. Samuels GJ, Ismaiel A (2009). Trichoderma evansii and T. lieckfeldtiae: two new T. hamatum-like species. Mycologia. 101:142-152.
  64. Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP. 2011. Trichoderma: the genomics of opportunistic success. Nat. Rev. Microbiol. 16:749-759.
  65. Lorito, M., 1998. Chitinolytic enzymes and their genes. In: Harman, G.E., Kubicek, C.P. (Eds.), Trichoderma and Gliocladium, Vol. 2. Taylor and Francis Ltd., London, pp. 73-99.
  66. Lorito, M., Hayes, C.K., Di Pietro, A., Woo, S.L., Harman, G.E., 1994a. Purification, characterization and synergistic activity of a glucan 1,3-b-glucosidase and an N-acetyl-b-glucosaminidase from Trichoderma harzianum. Phytopathology 84, 398-405.
  67. Lorito, M., Farkas, V., Rebuffat, S., Bodo, B., Kubicek, C.P., 1996b.Cell wall synthesis is a major target of mycoparasitic antagonism by Trichoderma harzianum. Journal of Bacteriology 178:6382-6385.
  68. Harman, G.E., Kubicek, C.P., 1998. Trichoderma and Gliocladium. Taylor & Francis, London, 278.
  69. Baek, J.M., Howell, C.R., Kenerley, C.M., 1999. The role of an extracellular chitinase from Trichoderma virens Gv29-8 in the biocontrol of Rhizoctonia solani. Current genetics 35, 41-50.
  70. Carsolio, C., Benhamou, N., Haran, S., Cortes, C., Gutierrez, A., Chet, I., Herrera-Estrella, A., 1999. Role of the Trichoderma harzianum endochitinase gene,ech4, in mycoparasitism. Applied Environmental Microbiology 65, 929-935.
  71. Woo, S.L., Donzelli, B., Scala, F., Mach, R., Harman, G.E., Kubicek, C.P.,Del Sorbo, G., Lorito, M., 1999. Disruption of the ech42 (endochitinase-encoding) gene affect biocontrol activity in Trichoderma harzianum P1.Molecular Plant-Microbe Interaction 12, 419-429.
  72. Kullnig, C., Mach, R.L., Lorito, M., Kubicek, C.P., 2000. Enzyme diffusion from Trichoderma atroviride(T. harzianumP1) to Rhizoctonia solani is a prerequisite for triggering of Trichoderma ech42 gene expression before mycoparasitic contact. Applied Environmental Microbiology 66: 2232-2234.
  73. Kubicek, C.P., Mach, R.L., Peterbauer, C.K., Lorito, M., 2001. Trichoderma: from genes to biocontrol. Journal of Plant Pathology 83: 11-23.
  74. Tronsmo, A., 1991. Biological and integrated controls of Botrytis cinerea on apple with Trichoderma harzianum. Biological Control 1, 59-62.
  75. Lorito, M., Harman, G.E., Hayes, C.K., Broadway, R.M., Tronsmo, A.,Woo, S.L., Di Pietro, A., 1993. Chitinolytic enzymes produced by Trichoderma harzianum: antifungal activity of purified endochitinase and chitobiosidase. Phytopathology 83, 302-307.
  76. Lorito, M., Scala, F., 1999. Microbial genes expressed in transgenic plants to improve disease resistance. Journal of Plant Pathology 81, 73-88.
  77. Woo, S.L., Lorito, M., 2007. Exploiting the interactions between fungal antagonists, pathogens and the plant for biocontrol. In: Vurro, M.,Gressel, J. (Eds.), Novel Biotechnologies for Biocontrol Agent Enhancement and Management. IOS, Springer Press, Amsterdam, Netherlands, pp. 107-130 (Chapter 6).
  78. Mach, R.L., Peterbauer, C.K., Payer, K., Jaksits, S., Woo, S.L., Zeilinger, S.,Kullnig, C.M., Lorito, M., Kubicek,C.P., 1999. Expression of two major chitinase genes of Trichoderma atroviride (T. harzianum P1) is triggered by different regulatory signals. Applied Environmental Microbiology. 65:1858-1863.
  79. Lorito, M., Peterbauer, C., Hayes, C.K., Harman, G.E., 1994b.Synergistic interaction between fungal cell wall degrading enzymes and different antifungal compounds enhances inhibition of spore germination. Microbiology. 140: 623-629.
  80. Yedidia, I., Shoresh, M., Kerem, Z., Benhamou, N.,Kapulnik, Y., Chet, I.,2003. Concomitant induction of systemic resistance to Pseudomonas syringae pv. Lachrymans in cucumber by Trichoderma asperellum (T-203) and accumulation of phytoalexins. Applied Environmental Microbiology. 69: 7343-7353.
  81. Hanson, L.E., Howell, C.R., 2004. Elicitors of plant defense responses from biocontrol strains of Trichoderma virens. Phytopathology. 94:171-176.
  82. Marra, R., Ambrosino, P., Carbone, V., Vinale, F., Woo, S.L., Ruocco, M.,Ciliento, R., Lanzuise, S., Ferraioli, S., Soriente, I., Gigante, S.,Turra`, D., Fogliano, V., Scala, F., Lorito, M., 2006. Study of the three-way interaction between Trichoderma atroviride, plant and fungal pathogens by using a proteomic approach. Current Genetics. 50:307-321.
  83. Schuster A. and Schmoll M. 2010. Biology and biotechnology of Trichoderma. Appl. Microbiol. Biotechnol. 87: 789-799.
  84. Kowsari M., Motallebi M., Zamani R.M. 2014. Construction of new GFP-tagged fusants for Trichoderma harzianum with enhanced biocontrol activity. J. Plant Prot. Res. 54: 122-131.
  85. Sadowski C., Lenc L., Domoradzki M., Korpal W., Weiner W., Lukanowski A. 2006a. Studies on plant health in organic production of vegetable seeds. p. 410-411. In: Proc. European Joint Organic Congress, Odense, Denmark, 30-31 May 2006, 713 pp.
  86. Sadowski C., Lenc L., Korpal W. 2007. Badania nad mo?liwo?ci? ochrony buraka ?wik?owego przed chorobami grzy-bowymi w uprawie ekologicznej. Investigation on the possibility of protection of organically grown red beet against fungal diseases. J. Res. Appl. Agric. Eng. 52: 38-44.
  87. Dawidziuk A., Popiel D., J?dryczka M. 2013. The influence of Trichoderma species on Leptosphaeria maculans and L. biglobosa growth on agar media and in oilseed rape plants. Integrated Control in Oilseed Crops IOBC-WPRS Bulletin. 92: 119-126.
  88. El-Hassan S.A., Gowen S.R., Pembroke B. 2013. Use of Trichoderma hamatum for biocontrol of lentil vascular wilt disease: efficacy, mechanisms of interaction and future prospects. J. Plant Prot. Res. 53: 12-26.
  89. Sadowski C., Lenc L., Korpal W. 2006b. Z bada? nad otoczkowaniem nasion warzyw z wykorzystaniem Trichoderma viridei zdrowotno?ci? ro?lin w uprawie ekologicznej. Out of investigations of vegetable seed coating with Trichoderma viride and plant health in organic system . J. Res. Appl. Ag-ric. Eng. 51: 150-153.
  90. Kancelista A., Tril U., Stempniewicz R., Piegza M., Szczech M., Witkowska D. 2013. Application of lignocellulosic waste materials for the production and stabilization of Trichoderma biomass. Pol. J. Environ. Stud. 22: 1083-1090.
  91. Smoli?ska U., Kowalska B., Kowalczyk W., Szczech M. 2014. The use of agro-industrial wastes as carriers of Trichoderma fungi in the parsley cultivation. Sci. Hortic. 179: 1-8.
  92. Thrane C., Tronsmo A., Jensen D.F. 1997. Endo-1,3-?-glucanase and cellulose from Trichoderma harzianum: purification and partial characterization, induction of and biological activity against plant pathogenic Pythium spp. Europ. J. Plant Pathol.103: 331-344.
  93. Dengkolb T., Berg A., Gams W., Schlegel B., Grafe U. 2003. The occurrence of peptaibols and structurally related peptabiotics in fungi and their mass spectrometric identification via diagnostic fragment ions. J. Pept. Sci. 9: 666-678.
  94. Osbourn A. 2010. Secondary metabolic gene clusters: evolutionary toolkits for chemical innovation. Trends Genet. 26: 449-457.
  95. Hatvani L., Antal L., Manczinger L., Szekeres A., Druzhinina I.S., Kubicek C.P., Nagy E., Vagvolgyi C., Kredics L. 2007. Green mold diseases of Agaricus and Pleurotus spp. are caused by related but phylogenetically different Trichoderema species. Phytopathology 97: 532-537. 96.
  96. Szczech M., Staniaszek M., Habdes H., Ulinski Z., Szymanski J. 2008.Trichoderma spp. - the cause of green mold on Polish farms. Veg. Crops Res. Bull. 69: 105-114.
  97. Kredics L., Garcia Jimenez L., Nagimi S., Czifra D., Urban P., Manczinger L., Vagvolgyi C., Hatvani L. 2010. A challenge to mushroom growers, the green mould disease of cultivated champignons. p. 295-305. In: “Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology” (A. Mendez-Vilas, ed.). Microbiology Book Series 2 (1), Formatex, Badajoz, Spain, 788 pp.
  98. Sobieralski K., Siwulski M., B?aszczyk L., Fru?y?ska-J??wiak D., Lisiecka J. 2012b. The effect of infestation with isolates of Trichoderma sp. on mycelium growth and yielding in single-spore heterokaryotic cultures of Agaricus bisporus(Lange) Imbach. Acta Sci. Pol. - Hortorum Cultus. 11: 47-57.
  99. Gorski R., Sobieralski K., Siwulski M., Fr?szczak B., Sas-Golak I. 2014. The effect of Trichoderma isolates, from family mushroom growing farms, on the yield of four Agaricus bisporus(Lange) Imbach strains. J. Plant Prot. Res. 54: 102-105.
  100. Samuels G.J., Dodd S.L., Gams W., Castelbury L.A., Petrini O. 2002. Trichoderma species associated with the green mold epidemic of commercially grown Agaricus bisporus. Mycologia 94: 146-170.
  101. Williams J., Clarkson J.M., Mils P.R., Cooper R.M. 2003. Saprotrophic and mycoparasitic components of aggressiveness of Trichoderma harzianum groups toward the commercial mushroom Agaricus bisporus. Appl. Environ. Microbiol. 69: 4192-4199.
  102. Druzhinina I.S., Komon-Zelazowska M., Kredics L., Hatvani L., Antal Z., Belayneh T., Kubicek C.P. 2008. Alternative reproductive strategies of Hypocrea orientalis and genetically close but clonal Trichoderma longibrachiatum, both capable to cause invasive mycoses of humans. Microbiology 54: 3447-3459.
  103. Kredics L., Antal Z., Doczi I., Manczinger L., Kevei F., Nagy E. 2003. Clinical importance of the genus Trichoderma. A review. Acta Microbiol. Immunol. Hung. 50: 105-117.
  104. Kratzer C., Tobudic S., Schmoll M., Graninger W., Georgopoulos A. 2006. In vitro activity and synergism of amphotericin B, azoles and cationic antimicrobials against the emerging pathogen Trichoderma spp. J. Antimicrob. Chemother. 58: 1058-1061.
  105. Alanio A., Brethon B., Feuihade de Chauvin M., Kerviler E., Leblanc T., Lacroix C., Baruchel A., Menotti J. 2008. Invasive pulmonary infection due to Trichoderma longibrachiatum mimicking invasive Aspergillosis in a neutropenic patient successfully treated with voriconazole combined with caspofungin. Clin. Infect. Dis. 46: 116-118.
  106. Larsen F.O., Clementsen P., Hansen M., Maltbaek N., Ostenfeldt Larsen T., Nielsen K.F., Gravesen S., Skov P.S., Non S. 1998. Volatile compounds from the indoor mould Trichoderma viride cause histamine release from human bronchoalveolar cells. Inflamm. Res. 47: 55-56.
  107. Wilson, L.S. 1996. Biochemical and molecular characterization of Trichoderma spp. A thesis submitted in University of Auckland.
  108. Fletcher, J.T. 1990. Trichoderma and Penicillium disease of Agaricus bisporus. A literature review for the Horticultural Development Council, London, UK: ADAS.
  109. Nallanchakravarthula S, Mahmood S, Alstr?m S, Finlay RD. 2014. Influence of Soil Type, Cultivar and Verticillium dahliae on the Structure of the Root and Rhizosphere Soil Fungal Microbiome of Strawberry. PLoS ONE 9(10): e111455. doi:10.1371/journal.pone.0111455.
  110. Yang C, Crowley DE, Menge JA. 2001. 16S rDNA fingerprinting of rhizosphere bacterial communities associated with healthy and Phytophthora infected avocado roots. FEMS Microbiol Ecol 35: 129-136.
  111. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH. 2013. Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11: 789-799.
  112. Rao, D.L.N. (Ed.) Project Coordinator, AINP on Soil Biodiversity- Biofertilizers, ICAR-Indian Institute of Soil Science, Bhopal, pp 82.
  113. B?aszczyk L, Siwulski M, Sobieralski K , Lisiecka J, J?dryczka M . 2014. Trichoderma spp. - application and prospects for use in organic farming and industry. Journal of Plant Protection research. Vol. 54, No. 4. 309-317.
  114. Druzhinina I.S , Komon-Zelazowska M, Kredics L, Hatvani L , Antal Z, Belayneh T, Kubicek C.P. 2008. Alternative reproductive strategies of Hypocrea orientalis and genetically close but clonal Trichoderma longibrachiatum, both capable to cause invasive mycoses of humans. Microbiology 54 (11): 3447-3459.
  115. Kubicek C.P., Herrera-Estrella A., Seidl-Seiboth V., Martinez D.A., Druzhinina J.S. 2011. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol. 12 (4): R40.DOI: 10.1186/gb-2011-12-4-r40.
  116. Mukherjee P.K., Horwitz B.A., Kenerley C.M. 2012. Secondary metabolism in Trichoderma - a genomic perspective. Microbiology 158: 35-45.
  117. Brakhage A.A and Schroeckh V. 2011. Fungal secondary metabolites- strategies to activate silent gene clusters. Fungal Genet. Biol. 48: 15-22.
  118. Ben?tez T, Rinc?n A.M, Lim?n M.C and Cod?n A.C. 2004. Biocontrol mechanisms of Trichoderma Strains. International Microbiology. 7:249-260.
  119. Richter S, Cormican M. G, Pfaller M. A, Lee C. K, Gingrich R, Rinaldi M. G, and Sutton D. A.1999. Fatal disseminated Trichoderma longibrachiatum infection in an Adult bone marrow transplant patient: Species identification and review of the literature. J Clin Microbiol. 1999 Apr; 37: 1154-1160.

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Published

2017-08-31

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Research Articles

How to Cite

[1]
Priya Solanki, Srivathsa Nallanchakravarthula, " Beneficial and Harmful Aspects of Trichoderma : A Review, International Journal of Scientific Research in Science and Technology(IJSRST), Online ISSN : 2395-602X, Print ISSN : 2395-6011, Volume 3, Issue 6, pp.569-577, July-August-2017.