Trichoderma pp 125-147 | Cite as

Induced Immunity Developed by Trichoderma Species in Plants

  • B. N. Chakraborty
  • U. Chakraborty
  • K. Sunar
Part of the Rhizosphere Biology book series (RHBIO)


One of the most interesting and important microorganisms in nature is Trichoderma, which, from being a mycoparasitic biocontrol agent (BCA), has now emerged as one with multiple traits such as antagonism to pathogen, competition with pathogens for nutrients, induction of systemic resistance in the host, overall plant growth promotion and also alleviation of abiotic stresses. Besides, interestingly, though they were reported earlier as soil and root colonizers only, it is now evident that several species of Trichoderma are endophytic. Interactions between plant and Trichoderma involve recognition, penetration, attachment and colonization and, finally, nutrient transfer from the root. Appressoria-like structures have been reported to be formed by Trichoderma which helps in root penetration, and two proteins TasHyd1 and qid74 were found to mediate the attachment of appressoria to the roots. Trichoderma produces a large number of secondary metabolites such as xylanases, cellulases, polygalacturonases, cerato-platanins, swollenins, peptaibols, 6-pentyl-α-pyrones and trichothecenes. These secondary metabolites help Trichoderma in various capacities, such as cell wall-degrading enzymes, elicitors and antimicrobial compounds. Trichoderma can trigger plant resistance towards pathogen attack by inducing plant immune response. Trichoderma viride, T. harzianum, T. virens, T. aureoviride and T. asperellum are being used as microbial inducers of plant immunity. An immunity-inducing protein (Sm1/Ep11) of the cerato-platanin family and elicitor produced by Trichoderma increase the expression of genes involved in defence, which in turn induces immunity. Trichoderma spp. release microbe-associated molecular patterns (MAMPs) required for molecular recognition leading to a signal cascade within the plant involving signalling molecules such as salicylic acid (SA), jasmonate (JA) and ethylene (ET). The defence responses triggered by Trichoderma, both locally and systemically, include enhanced accumulation of PR proteins, phytoalexins and terpenoids and enhanced activities of several enzymes such as phenylalanine ammonia lyase, peroxidase, polyphenol oxidase and lipoxygenase. Activation of such defence responses finally leads to crop protection through induced resistance.


Biocontrol Secondary metabolites Plant immunity Induced resistance Defence enzymes 


  1. Abbas A, Jiang D, Fu Y (2017) Trichoderma spp. as antagonist of Rhizoctonia solani. J Plant Pathol Microbiol 8:402Google Scholar
  2. Ahmed AS, Sanchez CP, Candela ME (2000) Evaluation of induction of systemic resistance in pepper plants (Capsicum annuum) to Phytophthora capsici using Trichoderma harzianum and its relation with capsidiol accumulation. Eur J Plant Pathol 106:817–824CrossRefGoogle Scholar
  3. Alfano G, Ivey ML, Cakir C, Bos JIB, Miller SA, Madden LV, Kamoun S, Hoitnik HA (2007) Systemic modulation of gene expression in tomato by Trichoderma hamatum 382. Phytopathology 97:429–437PubMedCrossRefGoogle Scholar
  4. Allay S, Chakraborty BN (2010) Activation of defence response of mandarin plats against Fusarium root rot diseases using Glomus mosseae and Trichoderma hamatum. J Mycol Plant Pathol 40:499–511Google Scholar
  5. Allay S, Chakraborty BN (2013) Induction of resistance in Citrus reticulata against Fusarium solani by dual application of AMF and Trichoderma asperellum. Int. J. Bioresour Stress Manag 4:588–592Google Scholar
  6. Bae H, Sicher RC, Kim MS, Kim SH, Strem MD (2009) The beneficial endophyte Trichoderma hamatum isolate DIS219b promotes growth and delays the onset of the drought response in Theobroma cacao. J Exp Bot 60:3279–3295PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bigirimana J, de Meyer G, Poppe J, Elad Y, Hofte M (1997) Induction of systemic resistance on bean (Phaseolus vulgaris) by Trichoderma harzianum. Med Fac Landbouww Univ Gent 62:1001–1007Google Scholar
  8. Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern recognition receptors. Annu Rev Plant Biol 60:379–406PubMedCrossRefGoogle Scholar
  9. Brotman Y, Briff E, Viterbo A, Chet I (2008) Role of swollenin, an expansin-like protein from Trichoderma, in plant root colonization. Plant Physiol 147:779–789PubMedPubMedCentralCrossRefGoogle Scholar
  10. Brotman Y, Lisec J, Méret M, Chet I, Willmitzer L, Viterbo A (2012) Transcript and metabolite analysis of the Trichoderma-induced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana. Microbiology 158:139–146PubMedCrossRefGoogle Scholar
  11. Brotman Y, Landau U, Cuadros-Inostroza A (2013) Trichoderma plant root colonization: escaping early plant defence responses and activation of the antioxidant machinery for saline stress tolerance. PLoS Pathog 9:e1003221PubMedPubMedCentralCrossRefGoogle Scholar
  12. Cardoza RE, Malmierca MG, Hermosa MR, Alexander NJ, McCormick SP, Proctor RH, Tijerino AM, Rumbero A, Monte E, Gutiérrez S (2011) Identification of loci and functional characterization of trichothecene biosynthesis genes in filamentous fungi of the genus Trichoderma. Appl Environ Microbiol 77:4867–4877PubMedPubMedCentralCrossRefGoogle Scholar
  13. Casas-Flores S, Rios-Momberg M, Rosales-Saavedra T, Martinez-Hernandez P, Olmedo-Monfil V, Herrera-Estrella A (2006) Cross talk between a fungal blue-light perception system and the cyclic AMP signaling pathway. Eukaryot Cell 5:499–506PubMedPubMedCentralCrossRefGoogle Scholar
  14. Chacón MR, Rodriguez-Galan O, Benítez T, Sousa S, Rey M, Llobell A, Delgado-Jarana J (2007) Microscopic and transcriptome analyses of early colonization of tomato roots by Trichoderma harzianum. Int Microbiol 10:19–27PubMedGoogle Scholar
  15. Chakraborty BN (2005a) Antimicrobial proteins in plant defence. In: Chakravorti SS (ed) New perspectives in the frontiers of chemical research. Royal Society of Chemistry (EIS), Kolkata, pp 470–483Google Scholar
  16. Chakraborty U (2005b) Formation and scavenging of active oxygen species in plants. In: Chakravorti SS (ed) New perspectives in the frontiers of chemical research. Royal Society of Chemistry (EIS), Kolkata, pp 497–507Google Scholar
  17. Chakraborty BN (2012) Recognition of fungi and activation of defence responses in plants. In: Sigh HP, Chowdappa P, Chakraborty BN, Podile AR (eds) Molecular approaches for plant fungal disease management. Westville Publishing House, New Delhi, pp 70–95Google Scholar
  18. Chakraborty BN (2016) Scoping the potential uses of beneficial microorganisms for biopesticide industry and entrepreneurship development in crop protection. In: Chowdappa P, Sharma P, Singh D, Misra AK (eds) Perspectives of Plant Pathology in genomic era. Indian Phytopathological Society, IARI, New Delhi, pp 607–627Google Scholar
  19. Chakraborty BN, Chakraborty U (2008) Involvement of salicylic acid in plant defence against stresses. In: Khan NA, Singh S (eds) Abiotic stresses in plants. International Publishers, New Delhi, pp 233–246Google Scholar
  20. Chakraborty BN, Chakraborty U (2018) Tea diseases: early detection and their management strategies. In: Das S, Dutta S, Chakraborty BN, Singh D (eds) Recent approaches for management of plant diseases. Indian Phytopathological Society, IARI, New Delhi, pp 175–208Google Scholar
  21. Chakraborty BN, Sharma M (2008) Pathogenesis related proteins in plant defence. In: Reddy SM, Gour HN (eds) Review of plant pathology, vol 4. Scientific Publishers, Jodhpur, pp 105–138Google Scholar
  22. Chakraborty BN, Chakraborty U, Dey PL (2011) Potential application of Trichoderma as biocontrol agents, their molecular characterization and diversity analysis. In: Singh A (ed) Plant diseases and their biological control. Aavishkar Publishers, Jaipur, pp 186–216Google Scholar
  23. Chakraborty BN, Chakraborty U, Sunar K, Dey PL (2014) Harnessing beneficial microbial resources for crop improvement. In: Sigh DP, Singh HB (eds) Trends in soil Microbial ecology. Studium Press LLC, Houston, TX, pp 175–201Google Scholar
  24. Chakraborty BN, Chakraborty U, Allay S (2019) Wilt root rot complex in mandarin plants and activation of defence against pathogen. In: Bhattacharyya A, Chakraborty BN, Pandey RN, Singh D, Dubey SC (eds) Wilt diseases of crops. Indian Phytopathological Society, IARI, New Delhi, pp 293–321Google Scholar
  25. Chowdhury AK, Debnath A, Roy A, Bhattacharya PM, Chattopadhyay C (2017) Biological control in 21st century: opportunities and challenges in subsistence farming system in India. In: Pandey RN, Chakraborty BN, Singh D, Sharma P (eds) Microbial antagonists: role in biological control of plant diseases. Indian Phytopathological Society, IARI, New Delhi, pp 39–66Google Scholar
  26. Cong D, Li Y, Xian H (2012) Purification, renaturation and characterization of chitinase gene from Trichoderma asperellum. Chin Agric Sci Bull 28:34–38Google Scholar
  27. Contreras-Cornejo HA, Macías-Rodríguez L, Cortés-Penagos C, López-Bucio J (2009) Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol 149:1579–1592PubMedPubMedCentralCrossRefGoogle Scholar
  28. Contreras-Cornejo HA, Macías-Rodríguez L, Beltrán-Peña E, Herrera-Estrella A, López-Bucio J (2011) Trichoderma-induced plant immunity likely involves both hormonal and camalexin dependent mechanisms in Arabidopsis thaliana and confers resistance against necrotrophic fungus Botrytis cinerea. Plant Signal Behav 6:1554–1563PubMedPubMedCentralCrossRefGoogle Scholar
  29. Contreras-Cornejo HA, Macías-Rodríguez L, Del-Val E, Larsen J (2016) Ecological functions of Trichoderma spp. and their secondary metabolites in the rhizosphere: interactions with plants. FEMS Microbiol Ecol 92:fiw036PubMedCrossRefGoogle Scholar
  30. De Lorenzo G, Brutus A, Savatin DV, Sicilia F, Cervone F (2011) Engineering plant resistance by constructing chimeric receptors that recognize damage-associated molecular patterns (DAMPs). FEBS Lett 585:1521–1528PubMedCrossRefGoogle Scholar
  31. De Meyer G, Bigirimana J, Elad Y, Hofte M (1998) Induced systemic resistance in Trichoderma harzianum T39 biocontrol of Botrytis cinerea. Eur J Plant Pathol 104:279–286CrossRefGoogle Scholar
  32. Djonovic S, Pozo MJ, Dangott LJ, Howell CR, Kenerley CM (2006) Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defence responses and systemic resistance. Mol Plant Microbe Interact 19:838–853PubMedCrossRefGoogle Scholar
  33. Djonovic S, Vargas WA, Kolomiets MV, Horndeski M, Wiest A, Kenerley CM (2007) A proteinaceous elicitor Sm1from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol 145:875–899PubMedPubMedCentralCrossRefGoogle Scholar
  34. Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A (2011) Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9:749–759PubMedCrossRefGoogle Scholar
  35. Freitas RS, Steindorff AS, Ramada MH, de Siqueira SJ, Noronha EF, Ulhoa CJ (2014) Cloning and characterization of a protein elicitor Sm1 gene from Trichoderma harzianum. Biotechnol Lett 36:783–788PubMedCrossRefGoogle Scholar
  36. Godio RP, Fouces R, Martin JF (2007) A squalene epoxidase is involved in biosynthesis of both the antitumor compound Clavaric acid and Sterols in the Basidiomycete H. sublateritium. Chem Biol 14:1334–1346PubMedCrossRefGoogle Scholar
  37. Gulijimila M, Fan HJ, Liu ZH, Wang N, Dou K, Huang Y, Wang ZY (2012) Cloning and sequence analysis of small molecular hydrophobin protein hyb2 gene from Trichoderma asperellum T4. Chin Agric Sci Bull 28:85–91Google Scholar
  38. Hanson LE, Howell CR (2004) Elicitors of plant defence responses from biocontrol strains of Trichoderma virens. Phytopathology 94:171–176PubMedCrossRefGoogle Scholar
  39. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species-opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56PubMedCrossRefGoogle Scholar
  40. Hermosa R, Botella L, Keck E, Jiménez JA, Montero-Barrientos M, Arbona V, Gómez-Cadenas A, Monte E, Nicolás C (2011) The overexpression in Arabidopsis thaliana of a Trichoderma harzianum gene that modulates glucosidase activity, and enhances tolerance to salt and osmotic stresses. J Plant Physiol 168:1295–1302PubMedCrossRefGoogle Scholar
  41. Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25PubMedCrossRefGoogle Scholar
  42. Hermosa R, Belén Rubio M, Cardoza RE, Nicolás C, Monte E, Gutiérrez S (2013) The contribution of Trichoderma to balancing the costs of plant growth and defence. Int Microbiol 16:69–80PubMedGoogle Scholar
  43. Hidangmayum A, Dwivedi P (2018) Plant responses to Trichoderma spp. and their tolerance to abiotic stresses: a review. J Pharma Phytochem 7:758–766Google Scholar
  44. Howell CR, Hanson LE, Stipanovic RD, Puckhaber LS (2000) Induction of terpenoid synthesis in cotton roots and control of Rhizoctonia solani by seed treatment with Trichoderma virens. Phytopathology 90:248–252PubMedCrossRefGoogle Scholar
  45. Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedPubMedCentralCrossRefGoogle Scholar
  46. Kashyap PL, Kumar S, Srivastava AK (2017) Nano diagnostics for plant pathogens. Environ Chem Lett 15:7–13CrossRefGoogle Scholar
  47. Kubicek CP, Herrera-Estrella A, Seidl-Seiboth V et al (2011) Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol 12:R40PubMedPubMedCentralCrossRefGoogle Scholar
  48. Levy NO, Meller HY, Haile ZM, Elad Y, David E, Jurkevitch E, Katan J (2015) Induced resistance to foliar diseases by soil solarization and Trichoderma harzianum. Plant Pathol 64:365–374CrossRefGoogle Scholar
  49. Li MF, Li GH, Ke-Qin Zhang KQ (2019) Non-volatile metabolites from Trichoderma spp. Metabolites 9:58PubMedCentralCrossRefGoogle Scholar
  50. Lopez Mondejar R, Ros M, Pascual JA (2011) Mycoparasitism-related genes expression of Trichoderma harzianum isolates to evaluate their efficacy as biological control agent. Biol Control 56:59–66CrossRefGoogle Scholar
  51. López-Bucio J, Pelagio-Flores R, Herrera-Estrella A (2015) Trichoderma as biostimulant: exploiting the multilevel properties of a plant beneficial fungus. Sci Hortic 196:109–123CrossRefGoogle Scholar
  52. Luo Y, Zhang DD, Dong XW, Zhao PB, Chen LL, Song XY, Wang XJ, Chen XL, Shi M, Zhang YZ (2010) Antimicrobial peptaibols induce defence responses and systemic resistance in tobacco against tobacco mosaic virus. FEMS Microbiol Lett 313:120–126PubMedCrossRefGoogle Scholar
  53. Malmierca MG, Cardoza RE, Alexander NJ, McCormick SP, Hermosa R, Monte E, Gutiérrez S (2012) Involvement of Trichoderma trichothecenes in the biocontrol activity and induction of plant defence-related genes. Appl Environ Microbiol 78:4856–4868PubMedPubMedCentralCrossRefGoogle Scholar
  54. Malmierca MG, Cardoza RE, Alexander NJ, McCormick SP, Collado IG, Hermosa R, Monte E, Gutiérrez S (2013) Relevance of trichothecenes in fungal physiology: disruption of tri5 in Trichoderma arundinaceum. Fungal Genet Biol 53:22–33PubMedCrossRefGoogle Scholar
  55. Marra R, Ambosino P, Carbone V, Vinale F, Woo SL (2006) Study of the three-way interaction between Trichoderma atroviride, plant and fungal pathogens using a proteome approach. Curr Genet 50:307–321PubMedCrossRefGoogle Scholar
  56. Martinez C, Blanc F, Le Claire E, Besnard O, Nicole M, Baccou JC (2001) Salicylic acid and ethylene pathways are differentially activated in melon cotyledons by active or heat-denatured cellulase from Trichoderma longibrachiatum. Plant Physiol 127:334–344PubMedPubMedCentralCrossRefGoogle Scholar
  57. Masunaka A, Hyakumachi M, Takenaka S (2011) Plant growth promoting fungus, Trichoderma koningii suppresses isoflavonoid phytoalexin vestitol production for colonization on/in the roots of Lotus japonicus. Microb Environ 26:128–134CrossRefGoogle Scholar
  58. Matarasso N, Schuster S, Avni A (2005) A novel plant cysteine protease has a dual function as a regulator of 1-aminocyclopropane-1-carboxylic acid synthase gene expression. Plant Cell 17:1205–1216PubMedPubMedCentralCrossRefGoogle Scholar
  59. Mathys J, De Cremer K, Timmermans P, Van Kerckhove S, Lievens B, Vanhaecke M, Cammue BP, De Coninck B (2012) Genome-wide characterization of ISR induced in Arabidopsis thaliana by Trichoderma hamatum T382 against Botrytis cinerea infection. Front Plant Sci 3:108PubMedPubMedCentralCrossRefGoogle Scholar
  60. Meller HY, Haile MZ, David D, Borenstein M, Shulchani R, Elad Y (2013) Induced systemic resistance against grey mould in tomato (Solanum lycopersicum) by benzothiadiazole and Trichoderma harzianum T39. Phytopathology 104:150–157Google Scholar
  61. Mendoza-Mendoza A, Pozo MJ, Grzegorski D, Martinez P, Garcia JM, Olmedo-Monfil V, Cortes C, Kenerly C, Herrera-Estrella A (2003) Enhanced biocontrol activity of Trichoderma through inactivation of a mitogen- activated protein kinase. Proc Natl Acad Sci U S A 100:15965–15970PubMedPubMedCentralCrossRefGoogle Scholar
  62. Mendoza-Mendoza A, Rosales-Saavedra T, Cortes C (2007) The MAP kinase TVK1 regulates conidiation, hydrophobicity and the expression of genes encoding cell wall proteins in the fungus Trichoderma virens. Microbiology 153:2137–2147PubMedCrossRefGoogle Scholar
  63. Migheli Q, Gonzalez-Candelas L, Dealessi L, Camponogara A, Ramon-Vidal D (1998) Transformants of Trichoderma longibrachiatum overexpressing the beta-1,4-endoglucanase gene egl1 show enhanced biocontrol of Pythium ultimum on cucumber. Phytopathology 8:673–677CrossRefGoogle Scholar
  64. Morán-Diez E, Hermosa R, Ambrosino P, Cardoza RE, Gutiérrez S, Lorito M, Monte E (2009) The ThPG1 endopolygalacturonase is required for the Trichoderma harzianum-plant beneficial interaction. Mol Plant Microbe Interact 22:1021–1031PubMedCrossRefGoogle Scholar
  65. Mukherjee PK, Latha J, Hadar R, Horwitz BA (2003) TmkA, a mitogen-activated protein kinase of Trichoderma virens, is involved in biocontrol properties and repression of conidiation in the dark. Eukaryot Cell 2:446–455PubMedPubMedCentralCrossRefGoogle Scholar
  66. Mukherjee PK, Latha J, Hadar R, Horwitz BA (2004) Role of two G-protein alpha subunits, TgaA and TgaB, in the antagonism of plant pathogens by Trichoderma virens. Appl Environ Microbiol 70:542–549PubMedPubMedCentralCrossRefGoogle Scholar
  67. Mukherjee M, Mukherjee PK, Kale SP (2007) cAMP signalling is involved in growth, germination, mycoparasitism and secondary metabolism in Trichoderma virens. Microbiology 153:1734–1742PubMedCrossRefGoogle Scholar
  68. Mukherjee PK, Horwitz BA, Kenerley CM (2012) Secondary metabolism in Trichoderma: a genomic perspective. Microbiology 158:35–45PubMedCrossRefGoogle Scholar
  69. Nemcovic M, Farkas V (1998) Stimulation of conidiation by derivatives of cAMP in Trichoderma viride. Folia Microbiol 43:399–402CrossRefGoogle Scholar
  70. Nielsen KF, Gräfenhan T, Zafari D, Thrane U (2005) Trichothecene production by Trichoderma brevicompactum. J Agric Food Chem 53:8190–8196PubMedCrossRefGoogle Scholar
  71. Nogueira KMV, Costa MDN, de Paula RG, Mendonça-Natividade FC, Ricci-Azevedo R, Nascimento SRN (2015) Evidence of cAMP involvement in cellobiohydrolase expression and secretion by Trichoderma reesei in presence of the inducer sophorose. BMC Microbiol 15:195PubMedPubMedCentralCrossRefGoogle Scholar
  72. Perazzolli M, Roatti B, Bozza E, Pertot I (2011) Trichoderma harzianum T39 induces resistance against downy mildew by priming for defence without costs for grapevine. Biol Control 58:74–82CrossRefGoogle Scholar
  73. Perazzolli M, Moretto M, Fontana P, Ferrarini A, Velasco R, Moser C, Delledonne M, Pertot I (2012) Downy mildew resistance induced by Trichoderma harzianum T39 in susceptible grapevines partially mimics transcriptional changes of resistant genotypes. BMC Genomics 13:660PubMedPubMedCentralCrossRefGoogle Scholar
  74. Petutschnig EK, Jones AME, Serazetdinova L, Lipka U, Lipka V (2010) The lysin motif receptor-like kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J Biol Chem 285:28902–28911PubMedPubMedCentralCrossRefGoogle Scholar
  75. Piel J, Atzorn R, Gäbler R, Kühnemann F, Boland W (1997) Cellulysin from the plant parasitic fungus Trichoderma viride elicits volatile biosynthesis in higher plants via the octadecanoid signalling cascade. FEBS Lett 416:143–148PubMedCrossRefGoogle Scholar
  76. Pineda A, Zheng SJ, Van Loon JJA, Pieterse CMJ, Dicke M (2010) Helping plants to deal with insects: the beneficial soil-borne microbes. Trends Plant Sci 15:507–514PubMedCrossRefGoogle Scholar
  77. Pozo MJ, Baek JM, García JM, Kenerley CM (2004) Functional analysis of tvsp1, a serine protease-encoding gene in the biocontrol agent Trichoderma virens. Fungal Genet Biol 41:336–348PubMedCrossRefGoogle Scholar
  78. Reithner B, Brunner K, Schuhmacher R, Peissl I, Seidl V, Krska R, Zeilinger S (2005) The G protein alpha subunit Tga1 of Trichoderma atroviride is involved in chitinase formation and differential production of antifungal metabolites. Fungal Genet Biol 42:749–760PubMedCrossRefGoogle Scholar
  79. Reithner B, Schuhmacher R, Stoppacher N, Pucher M, Brunner K, Zeilinger S (2007) Signaling via the Trichoderma atroviride mitogen-activated protein kinase Tmk1 differentially affects mycoparasitism and plant protection. Fungal Genet Biol 44:1123–1133PubMedPubMedCentralCrossRefGoogle Scholar
  80. Rocha-Ramirez V, Omero C, Chet I, Horwitz BA, Herrera-Estrella A (2002) Trichoderma atroviride G-protein alpha-subunit gene tga1 is involved in mycoparasitic coiling and conidiation. Eukaryot Cell 1:594–605PubMedPubMedCentralCrossRefGoogle Scholar
  81. Ron M, Avni A (2004) The receptor for the fungal elicitor ethylene- inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16:1604–1615PubMedPubMedCentralCrossRefGoogle Scholar
  82. Rosado IV, Rey M, Codón AC, Govantes J, Moreno-Mateos MA, Benítez T (2007) QID74 cell wall protein of Trichoderma harzianum is involved in cell protection and adherence to hydrophobic surfaces. Fungal Genet Biol 44:950–964PubMedCrossRefGoogle Scholar
  83. Rotblat B, Enshell-Seijffers D, Gershoni JM, Schuster S, Avni A (2002) Identification of an essential component of the elicitation active site of the EIX protein elicitor. Plant J 32:1049–1055PubMedCrossRefGoogle Scholar
  84. Rubio MB, Hermosa R, Reino JL, Collado IG, Monte E (2009) Thctf1 transcription factor of Trichoderma harzianum is involved in 6-pentyl80 2H-pyran-2-one production and antifungal activity. Fungal Genet Biol 46:17–27PubMedCrossRefGoogle Scholar
  85. Ruiz N, Wielgosz-Collin G, Poirier L, Grovel O, Petit KE, Mohamed-Benkada M, Pont TR, Bissett J, Vérité P, Barnathan G, Pouchus YF (2007) New Trichobrachins,11-residue peptaibols from a marine strain of Trichoderma longibrachiatum. Peptides 28:1351–1358PubMedCrossRefGoogle Scholar
  86. Salas-Marina MA, Silva-Flores MA, Uresti-Rivera EE, Castro-Longoria E, Harrera-Estrella A, Casas-Flores S (2011) Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance through jasmonate and salicylate pathways. Eur J Plant Pathol 131:15–26CrossRefGoogle Scholar
  87. Salas-Marina MA, Isordia-Jasso M, Islas-Osuna MA, Delgado-Sánchez P, Jiménez-Bremont JF, Rodríguez-Kessler M, Rosales-Saavedra MT, Herrera-Estrella A, Casas-Flores S (2015) The Epl1 and Sm1 proteins from Trichoderma atroviride and Trichoderma virens differentially modulate systemic disease resistance against different life style pathogens in Solanum lycopersicum. Front Plant Sci 23:77Google Scholar
  88. Samolski I, Rincón A, Pinzón LM (2012) The qid74 gene from Trichoderma harzianum has a role in root architecture and plant biofertilization. Microbiology 158:129–138PubMedCrossRefGoogle Scholar
  89. Seaman A (2003) Efficacy of OMRI-approved products for tomato foliar disease control. NY State Integr Pest Manag Progr Publ 129:164–167Google Scholar
  90. Segarra G, Casanova E, Bellido D (2007) Proteome, salicylic acid, and jasmonic acid changes in cucumber plants inoculated with Trichoderma asperellum strain T34. Proteomics 7:3943–3952PubMedCrossRefGoogle Scholar
  91. Seidl V, Schmoll M, Scherm B, Balmas V, Seiboth B, Migheli Q, Kubicek CP (2006) Antagonism of Pythium blight of zucchini by Hypocrea jecorina does not require cellulase gene expression but is improved by carbon catabolite derepression. FEMS Microbiol Lett 257:145–151PubMedCrossRefGoogle Scholar
  92. Sesták S, Farkas V (1993) Metabolic regulation of endoglucanase synthesis in Trichoderma reesei: participation of cyclic AMP and glucose-6-phosphate. Can J Microbiol 39:342–347PubMedCrossRefGoogle Scholar
  93. Sharma P, Kumar PV, Ramesh R, Saravanan K, Deep S, Shrama M, Mahesh S, Singh D (2011) Biocontrol genes from Trichoderma species: a review. Afr J Biotech 10(86):19898–19907Google Scholar
  94. Shoresh M, Harman GE (2008a) The relationship between increased growth and resistance induced in plants by root colonizing microbes. Plant Signal Behav 3:737–739PubMedPubMedCentralCrossRefGoogle Scholar
  95. Shoresh M, Harman GE (2008b) The molecular basis of shoot responses of maize seedlings to Trichoderma harzianum T22 inoculation of the root: a proteomic approach. Plant Physiol 147:2147–2163PubMedPubMedCentralCrossRefGoogle Scholar
  96. 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
  97. Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43PubMedCrossRefGoogle Scholar
  98. Simarmata T, Hersanti, Turmuktini T, Fitriatin BN, Setiawati MR, Purwanto (2015) Application of bioameliorant and biofertilizers to increase the soil health and rice productivity. Hayati J Biosci 23:181–184CrossRefGoogle Scholar
  99. Singh HB (2006) Trichoderma: a boon for biopesticide industry. J Mycol Plant Pathol 36:373–384Google Scholar
  100. Singh HB, Singh BN, Singh SP, Sarma BK (2012) Exploring different avenues of Trichoderma as a potent biofungicidal and plant growth promoting candidate – an overview. In: Bagyanarayana G, Gour HN, Manoharachary C, Kunwar IK (eds) Review of plant pathology, vol 5. Scientific Publishers, Jodhpur, pp 315–426Google Scholar
  101. Steyaert JM, Ridgway HJ, Elad Y, Stewart A (2003) Genetic basis of mycoparasitism: a mechanism of biological control by species of Trichoderma. J Crop Hortic Sci 31:281–291CrossRefGoogle Scholar
  102. Tijerino A, Cardoza RE, Moraga J, Malmierca MG, Vicente F, Aleu J, Collado IG, Gutiérrez S, Monte E, Hermosa R (2011) Overexpression of the trichodiene synthase gene tri5 increases trichodermin production and antimicrobial activity in Trichoderma brevicompactum. Fungal Genet Biol 48:285–296PubMedCrossRefGoogle Scholar
  103. Tisch D, Kubicek CP, Schmoll M (2011) New insights into the mechanism of light modulated signaling by heterotrimeric G-proteins: ENVOY acts on gna1 and gna3 and adjusts cAMP levels in Trichoderma reesei (Hypocrea jecorina). Fungal Genet Biol 48:631–640PubMedPubMedCentralCrossRefGoogle Scholar
  104. Tucci M, Ruocco M, De Masi L, De Palma M, Lorito M (2011) The beneficial effect of Trichoderma spp. on tomato is modulated by the plant genotype. Mol Plant Pathol 12:341–354PubMedCrossRefGoogle Scholar
  105. Van Wees SCM, van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448PubMedCrossRefGoogle Scholar
  106. Vargas WA, Mandawe JC, Kenerley CM (2009) Plant-derived sucrose is a key element in the symbiotic association between Trichoderma virens and maize plants. Plant Physiol 151:792–808PubMedPubMedCentralCrossRefGoogle Scholar
  107. Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Barbetti MJ, Li H, Woo SL, Lorito M (2008a) A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiol Mol Plant Pathol 72:80–86CrossRefGoogle Scholar
  108. Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Woo SL, Lorito M (2008b) Trichoderma-plant-pathogen interactions. Soil Biol Biochem 40:1–10CrossRefGoogle Scholar
  109. Viterbo A, Chet I (2006) TasHyd1, a new hydrophobin gene from the biocontrol agent Trichoderma asperellum, is involved in plant root colonization. Mol Plant Pathol 7:249–258PubMedCrossRefGoogle Scholar
  110. Viterbo A, Harel M, Horwitz BA, Chet I, Mukherjee PK (2005) Trichoderma mitogen activated protein kinase signalling is involved in induction of plant systemic resistance. Appl Environ Microbiol 71:6241–6246PubMedPubMedCentralCrossRefGoogle Scholar
  111. Viterbo A, Wiest A, Brotman Y, Chet I, Kenerley C (2007) The 18mer peptaibols from Trichoderma virens elicit plant defence responses. Mol Plant Pathol 8:737–746PubMedCrossRefGoogle Scholar
  112. Vizcaíno JA, Cardoza RE, Hauser M, Hermosa R, Rey M, Llobell A, Becker JM, Gutiérrez S, Monte E (2006) ThPTR2, a di/tri-peptide transporter gene from Trichoderma harzianum. Fungal Genet Biol 43:234–246PubMedCrossRefGoogle Scholar
  113. Walters DR, Ratsep J, Havis ND (2013) Controlling crop diseases using induced resistance: challenges for the future. J Exp Bot 64:1263–1280PubMedCrossRefGoogle Scholar
  114. Wu Q, Sun R, Ni M, Yu J, Li Y, Yu C, Dou K, Ren J, Chen J (2017) Identification of a novel fungus, Trichoderma asperellum GDFS1009, and comprehensive evaluation of its biocontrol efficacy. PLoS One 12(6):e0179957PubMedPubMedCentralCrossRefGoogle Scholar
  115. Yasmeen R, Siddiqui ZS (2017) Physiological responses of crop plants against Trichoderma harzianum in saline environment. Acta Bot Croat 76:154–162CrossRefGoogle Scholar
  116. 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. Appl Environ Microbiol 69:7343–7353PubMedPubMedCentralCrossRefGoogle Scholar
  117. Yoshioka Y, Ichikawa H, Naznin HA, Kogure A, Hyakumachi M (2012) Systemic resistance induced in Arabidopsis thaliana by Trichoderma asperellum SKT-1, a microbial pesticide of seedborne diseases of rice. Pest Manag Sci 68:60–66PubMedCrossRefGoogle Scholar
  118. Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant Microbe Interact 25:139–150PubMedCrossRefGoogle Scholar
  119. Zeilinger S, Omann M (2007) Trichoderma biocontrol: signal transduction pathways involved in host sensing and mycoparasitism. Gene Regul Syst Bio 8:227–234Google Scholar
  120. Zeilinger S, Gruber S, Bansal R, Mukherjee PK (2016) Secondary metabolism in Trichoderma-chemistry meets genomics. Fungal Biol Rev 30:74–90CrossRefGoogle Scholar
  121. Zhang J, Zhou JM (2010) Plant immunity triggered by microbial molecular signatures. Mol Plant 3:783–793PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2020

Authors and Affiliations

  • B. N. Chakraborty
    • 1
  • U. Chakraborty
    • 2
  • K. Sunar
    • 3
  1. 1.Department of Biological SciencesAliah UniversityKolkataIndia
  2. 2.Department of BotanyUniversity of North BengalSiliguriIndia
  3. 3.Department of BotanyBalurghat Mahila MahavidyalayaBalurghatIndia

Personalised recommendations