Skip to main content
SpringerLink
Log in

Trichoderma spp.: Efficient Inducers of Systemic Resistance in Plants

  • Chapter
  • First Online:
Microbial-mediated Induced Systemic Resistance in Plants

Abstract

Defense response in plants, triggered by biocontrol agents (BCAs), is an intensively investigated area. In recent past, various agriculturally important microorganisms have been identified and described as efficient inducer of systemic resistance in plant. Trichoderma spp. are established plant root colonizers and their biocontrol nature is primarily due to mycoparasitism and antibiosis mechanisms against various pathogens. Progress in research in plant immunity induced by beneficial microorganisms suggests that other than mycoparasitism and antibiosis, Trichoderma spp. are potent inducers of ISR in plants. There is need for more intensive studies aimed at gaining insight into the signal transduction pathways and defense responses elicited by Trichoderma. Furthermore, quick progress in molecular studies will lead to gain deeper insight into the regulation of complex interaction between plant and biocontrol agents and increase the efficiency of currently existing biocontrol strategies and plant disease management modules.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Institutional subscriptions

References

  • Abeysinghe (2009) Systemic resistance induced by Trichoderma harzianum RU01 against Uromyces appendiculatus on Phaseolus vulgaris. J Natl Sci Found Sri Lanka 37:203–207

    Google Scholar 

  • Ahmed AS, Sánchez 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 106:817–824

    Google Scholar 

  • Ahn IP, Lee SW, Suh SC (2007) Rhizobacteria-induced priming in Arabidopsis is dependent on ethylene, jasmonic acid, and NPR1. Mol Plant Microbe Interact 20:759–768

    CAS  PubMed  Google Scholar 

  • Alfano G, Ivey ML, Cakir C, Bos JIB, Miller SA, Madden LV, Kamoun S, Hoitink HAJ (2007) Systemic modulation of gene expression in tomato by Trichoderma hamatum 382. Phytopathology 97:429–437

    CAS  PubMed  Google Scholar 

  • Bae H, Roberts DP, Lim HS, Strem MD, Park SC, Ryu CM, Melnick RL, Bailey BA (2011) Endophytic Trichoderma isolates from tropical environments delay disease onset and induce resistance against Phytophthora capsici in hot pepper using multiple mechanisms. Mol Plant Microbe Interact 24:336–351

    CAS  PubMed  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The roles of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    CAS  PubMed  Google Scholar 

  • Bakker PAHM, Pieterse CMJ, Loon LCV (2007) Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97:239–243

    PubMed  Google Scholar 

  • Bigirimana J, De Meyer G, Poppe J, Elad Y, Höfte M (1997) Induction of systemic resistance on bean (Phaseolus vulgaris) by Trichoderma harzianum. Med Fac Landbouwwet Univ Gent 62:1001–1007

    Google Scholar 

  • Bisen K, Keswani C, Mishra S, Saxena A, Rakshit A, Singh HB (2015) Unrealized potential of seed biopriming for versatile agriculture. In: Rakshit A, Singh HB, Sen A (eds) Nutrient use efficiency: from basics to advances. Springer, New Delhi, pp 193–206

    Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Calderón AA, Zapata JM, Muñoz R, Pedreno MA, Barcelo AR (1993) Resveratrol production as a part of the hypersensitive-like response of grapevine cells to an elicitor from Trichoderma viride. New Phytol 124:455–463

    Google Scholar 

  • Carreras-Villaseñor N, Sánchez-Arreguín JA, Herrera-Estrella AH (2012) Trichoderma: sensing the environment for survival and dispersal. Microbiology 158:3–16

    PubMed  Google Scholar 

  • Chang PFL, Xu Y, Narasimhan ML, Cheah KT, Durzo MP, Damsz B, Kononowicz AK, Abad L, Hasegawa PM, Bressan RA (1997) Induction of pathogen resistance and pathogenesis-related genes in tobacco by a heat-stable Trichoderma mycelia extract and plant signal messengers. Physiol Plant 100:341–352

    CAS  Google Scholar 

  • Choudhary DK, Kasotia A, Jain S, Vaishnav A, Kumari S, Sharma KP, Varma A (2015) Bacterial-mediated tolerance and resistance to plants under abiotic and biotic stresses. J Plant Growth Regul: 1–25. DOI 10.1007/s00344-015-9521-x

    Google Scholar 

  • 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 149:1579–1592

    CAS  PubMed  PubMed Central  Google Scholar 

  • Contreras-Cornejo HA, Macias-Rodriguez L, Beltran-Pena E, Herrera-Estrella A, Lopez-Bucio J (2011) Trichoderma-induced plant immunity likely involves both hormonal and camalexin dependent mechanisms in Arabidopsis thaliana and confers resistance against necrotrophic fungi Botrytis cinerea. Plant Signal Behav 6:1554–1563

    CAS  PubMed  PubMed Central  Google Scholar 

  • De Bruijn I, De Kock MJD, Yang M, De Waard P, Van Beek TA, Raaijmakers JM (2007) Genome-based discovery, structure prediction and functional analysis of cyclic lipopeptide antibiotics in Pseudomonas species. Mol Microbiol 63:417–428

    PubMed  Google Scholar 

  • de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y, Bours R, van der Krol S, Shibuya N, Joosten MHAJ, Thomma BPHJ (2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953–955

    PubMed  Google Scholar 

  • De Meyer G, Bigirimana J, Elad Y, Höfte M (1998) Induced systemic resistance in Trichoderma harzianum T39 biocontrol of Botrytis cinerea. Eur J Plant Pathol 104:279–286

    Google Scholar 

  • de Oliveira AL, Gallo M, Pazzagli L, Benedetti CE, Cappugi G, Scala A, Pantera B, Spisni A, Pertinhez TA, Cicero DO (2011) The structure of the elicitor cerato-platanin (CP), the first member of the CP fungal protein family, reveals a double ψβ-barrel fold and carbohydrate binding. J Biol Chem 286:17560–17568

    PubMed  PubMed Central  Google Scholar 

  • Debode J, Maeyer KD, Perneel M, Pannecoucque J, Backer GD, Höfte M (2007) Biosurfactants are involved in the biological control of Verticillium microsclerotia by Pseudomonas spp. J Appl Microbiol 103:1184–1196

    CAS  PubMed  Google Scholar 

  • Djonovic S, Pozo MJ, Dangott LJ, Howell CR, Kenerley CM (2006) Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defense responses and systemic resistance. Mol Plant Microbe Interact 19:838–853

    CAS  PubMed  Google Scholar 

  • Djonovic S, Vargas WA, Kolomiets MV, Horndeski M, Wiest A, Kenerley CM (2007) A proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol 145:875–889

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 9:749–759

    CAS  PubMed  Google Scholar 

  • Duijff BJ, Pouhair D, Olivain C, Alabouvette C, Lemanceau P (1998) Implication of systemic induced resistance in the suppression of fusarium wilt of tomato by Pseudomonas fluorescens WCS417r and by nonpathogenic Fusarium oxysporum Fo47. Eur J Plant Pathol 104:903–910

    Google Scholar 

  • Engelberth J, Koch T, Schuler G, Bachmann N, Rechtenbach J, Boland W (2001) Ion channel-forming alamethicin is a potent elicitor of volatile biosynthesis and tendril coiling. Cross talk between jasmonate and salicylate signaling in lima bean. Plant Physiol 125:369–377

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fontenelle ADB, Guzzo SD, Lucon CMM, Harakava R (2011) Growth promotion and induction of resistance in tomato plant against Xanthomonas euvesicatoria and Alternaria solani by Trichoderma spp. Crop Prot 30:1492–1500

    Google Scholar 

  • Gallou A, Cranenbrouck S, Declerck S (2009) Trichoderma harzianum elicits defence response genes in roots of potato plantlets challenged by Rhizoctonia solani. Eur J Plant Pathol 124:219–230

    Google Scholar 

  • Gravel V, Antoun H, Tweddell RJ (2007) Growth stimulation and fruit yield improvement of greenhouse tomato plants by inoculation with Pseudomonas putida or Trichoderma atroviride: possible role of indole acetic acid (IAA). Soil Biol Biochem 39:1968–1977

    CAS  Google Scholar 

  • Handelsman J, Stabb EV (1996) Biocontrol of soilborne plant pathogens. Plant Cell 8:1855–1869

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56

    CAS  PubMed  Google Scholar 

  • Harman GE, Herrera-Estrella AH, Horwitz BA, Lorito M (2012) Special issue: Trichoderma–from basic biology to biotechnology. Microbiology 158:1–2

    CAS  PubMed  Google Scholar 

  • Hase S, Takahashi S, Takenaka S, Nakaho K, Arie T, Seo S, Ohashi Y, Takahashi H (2008) Involvement of jasmonic acid signalling in bacterial wilt disease resistance induced by biocontrol agent Pythium oligandrum in tomato. Plant Pathol 57:870–876

    CAS  Google Scholar 

  • Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25

    CAS  PubMed  Google Scholar 

  • Hossain MM, Sultana F, Kubota M, Hyakumachi M (2008) Differential inducible defense mechanisms against bacterial speck pathogen in Arabidopsis thaliana by plant-growth-promoting-fungus Penicillium sp. GP16–2 and its cell free filtrate. Plant Soil 304:227–239

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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 90:248–252

    CAS  PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    CAS  PubMed  Google Scholar 

  • Kamilova F, Lamers G, Lugtenberg B (2008) Biocontrol strain Pseudomonas fluorescens WCS365 inhibits germination of Fusarium oxysporum spores in tomato root exudate as well as subsequent formation of new spores. Environ Microbiol 10:2455–2461

    PubMed  Google Scholar 

  • Keswani C (2015) Proteomics studies of thermotolerant strain of Trichoderma spp. Ph.D. thesis, Banaras Hindu University, Varanasi, India

    Google Scholar 

  • Keswani C, Singh SP, Singh HB (2013) A superstar in biocontrol enterprise: Trichoderma spp. Biotechnol Today 3:27–30

    Google Scholar 

  • Keswani C, Mishra S, Sarma BK, Singh SP, Singh HB (2014) Unraveling the efficient application of secondary metabolites of various Trichoderma. Appl Microbiol Biotechnol 98:533–544

    CAS  PubMed  Google Scholar 

  • Khan J, Ooka JJ, Miller SA, Madden LV, Hoitink HAJ (2004) Systemic resistance induced by Trichoderma hamatum 382 in cucumber against Phytophthora crown rot and leaf blight. Plant Dis 88:280–286

    CAS  PubMed  Google Scholar 

  • Kloepper JW, Ryu CM, Zhang SA (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266

    CAS  PubMed  Google Scholar 

  • Korolev N, David DR, Elad Y (2008) The role of phytohormones in basal resistance and Trichoderma-induced systemic resistance to Botrytis cinerea in Arabidopsis thaliana. BioControl 53:667–683

    CAS  Google Scholar 

  • Leitgeb B, Szekeres A, Manczinger L, Vagvolgyl C, Kredics L (2007) The history of alamethicin: a review of most extensively studied peptaibol. Chem Biodivers 4:1027–1051

    CAS  PubMed  Google Scholar 

  • López-Mondéjar R, Ros M, Pascual JA (2011) Mycoparasitism-related genes expression of Trichoderma harzianum isolates to evaluate their efficacy as biological control agent. Biol Control 56:59–66

    Google Scholar 

  • Lorito M, Woo SL, Harman GE, Monte E (2010) Translational research on Trichoderma: from omics to the field. Annu Rev Phytopathol 48:395–417

    CAS  PubMed  Google Scholar 

  • Lugtenberg BJ, Dekkers L, Bloemberg GV (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol 39:461–490

    CAS  PubMed  Google Scholar 

  • Luo Y, Zhang DD, Dong XW, Zhao PB, Chen LL, Song XY, Wang XJ, Chen XL, Shi M, Zhang YZ (2010) Antimicrobial peptaibols induce defense responses and systemic resistance in tobacco against tobacco mosaic virus. FEMS Microbiol Lett 313:120–126

    CAS  PubMed  Google Scholar 

  • 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 defense-related genes. Appl Environ Microbiol 78:4856–4868

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 127:334–344

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 3:108

    PubMed  PubMed Central  Google Scholar 

  • Moran-Diez E, Hermosa R, Ambrosino P, Cardoza RE, Gutie’rrez S, Lorito M, Monte E (2009) The ThPG1 endopolygalacturonase is required for the Trichoderma harzianum–plant beneficial interaction. Mol Plant Microbe Interact 22:1021–1031

    CAS  PubMed  Google Scholar 

  • Mukherjee PK, Buensanteai N, Moran-Diez ME, Druzhinina IS, Kenerley CM (2012a) Functional analysis of non-ribosomal peptide synthetases (NRPSs) in Trichoderma virens reveals a polyketide synthase (PKS)/NRPS hybrid enzyme involved in induced systemic resistance response in maize. Microbiology 158:155–165

    CAS  PubMed  Google Scholar 

  • Mukherjee M, Mukherjee PK, Horwitz BA, Zachow C, Berg G, Zeilinger S (2012b) Trichoderma–plant–pathogen interactions: advances in genetics of biological control. Indian J Microbiol 52:522–529

    PubMed  PubMed Central  Google Scholar 

  • Paparu P, Dubois T, Coyne D, Viljoen A (2007) Defense-related gene expression in susceptible and tolerant bananas (Musa spp.) following inoculation with nonpathogenic Fusarium oxysporum endophytes and challenge with Radopholus similis. Physiol Mol Plant Pathol 71:149–157

    CAS  Google Scholar 

  • Perazzolli M, Dagostin S, Ferrari A, Elad Y, Pertot I (2008) Induction of systemic resistance against Plasmopara viticola in grapevine by Trichoderma harzianum T39 and benzothiadiazole. Biol Control 47:228–234

    CAS  Google Scholar 

  • Perazzolli M, Roatti B, Bozza E, Pertot I (2011) Trichoderma harzianum T39 induces resistance against downy mildew by priming for defense without costs for grapevine. Biol Control 58:74–82

    Google Scholar 

  • Pieterse CMJ, Van Wees SCM, Hoffland E, Van Pelt JA, Van Loon LC (1996) Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8:1225–1237

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316

    CAS  PubMed  Google Scholar 

  • Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    CAS  PubMed  Google Scholar 

  • 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 32:1049–1055

    CAS  PubMed  Google Scholar 

  • Salas-Marina MA, Silva-Flores MA, Uresti-Rivera EE, Castro-Longoria E, Herrera-Estrella A, Casas-Flores S (2011) Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance through jasmonic acid/ethylene and salicylic acid pathways. Eur J Plant Pathol 131:15–26

    CAS  Google Scholar 

  • Samolski I, Rincón AM, Pinzón 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

    CAS  PubMed  Google Scholar 

  • Saxena A, Raghuwanshi R, Singh HB (2015) Trichoderma species mediated differential tolerance against biotic stress of phytopathogens in Cicer arietinum L. J Basic Microbiol 55:195–206

    CAS  PubMed  Google Scholar 

  • Schwessinger B, Zipfel C (2008) News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr Opin Plant Biol 11:389–395

    CAS  PubMed  Google Scholar 

  • Segarra G, Casanova E, Bellido D, Odena MA, Oliveira E, Trillas I (2007) Proteome, salicylic acid, and jasmonic acid changes in cucumber plants inoculated with Trichoderma asperellum strain T34. Proteomics 7:3943–3952

    CAS  PubMed  Google Scholar 

  • Segarra G, Van der Ent S, Trillas I, Pieterse CMJ (2009) MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biol 11:90–96

    CAS  PubMed  Google Scholar 

  • Seidl V, Marchetti M, Schandl R, Allmaier G, Kubicek CP (2006) Epl1, the major secreted protein of Hypocrea atroviridis on glucose, is a member of a strongly conserved protein family comprising plant defense response elicitors. FEBS J 273:4346–4359

    CAS  PubMed  Google Scholar 

  • 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 95:76–84

    CAS  PubMed  Google Scholar 

  • Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43

    CAS  PubMed  Google Scholar 

  • Singh HB (2006) Trichoderma: a boon for biopesticides industry. J Mycol Plant Pathol 36:373–384

    Google Scholar 

  • Singh HB (2014) Management of plant pathogens with microorganisms. Proc Natl Acad Sci 80:443–454

    Google Scholar 

  • Singh HB, Singh BN, Singh SP, Sarma BK (2012) Exploring different avenues of Trichoderma as a potent bio-fungicidal and plant growth promoting candidate-an overview. Rev Plant Pathol 5:315–426

    Google Scholar 

  • Singh BN, Singh A, Singh BR, Singh HB (2014a) Trichoderma harzianum elicits induced resistance in sunflower challenged by Rhizoctonia solani. J Appl Microbiol 116:654–666

    CAS  PubMed  Google Scholar 

  • Singh HB, Singh A, Sarma BK, Upadhyay DN (2014b) Trichoderma viride 2% WP (Strain No. BHU-2953) formulation suppresses tomato wilt caused by Fusarium oxysporum f. sp. lycopersici and chilli damping-off caused by Pythium aphanidermatum effectively under different agroclimatic conditions. Int J Agric Environ Biotechnol 7:313–320

    Google Scholar 

  • Stein E, Molitor A, Kogel KH, Waller F (2008) Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1. Plant Cell Physiol 49:1747–1751

    CAS  PubMed  Google Scholar 

  • Stepanova AN, Yun J, Likhacheva AV, Alonso JM (2007) Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19:2169–2185

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ton J, Van Pelt JA, Van Loon LC, Pieterse CMJ (2002) Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis. Mol Plant Microbe Interact 15:27–34

    CAS  PubMed  Google Scholar 

  • 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 12:341–354

    CAS  PubMed  Google Scholar 

  • Van der Ent S, Verhagen BWM, Van Doorn R, Bakker D, Verlaan MG, Pel MJC, Joosten RG, Proveniers MCG, Van Loon LC, Ton J, Pieterse CMJ (2008) MYB72 is required in early signaling steps of rhizobacteria-induced systemic resistance in Arabidopsis. Plant Physiol 146:1293–1304

    PubMed  PubMed Central  Google Scholar 

  • Van Loon LC, Bakker PAHM (2006) Root-associated bacteria inducing systemic resistance. In: Gnanamanickam SS (ed) Plant-associated bacteria. Springer, Dordrecht, pp 269–316

    Google Scholar 

  • Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483

    PubMed  Google Scholar 

  • Van Loon LC, Bakker PAHM, Van der Heijdt WHW, Wendehenne D, Pugin A (2008) Early responses of tobacco suspension cells to rhizobacterial elicitors of induced systemic resistance. Mol Plant Microbe Interact 21:1609–1621

    PubMed  Google Scholar 

  • Van Wees SCM, Van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448

    PubMed  Google Scholar 

  • 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 151:792–808

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Barbetti MJ, Li H, Woo SL, Lorito M (2008) A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiol Mol Plant Pathol 72:80–86

    CAS  Google Scholar 

  • 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 7:249–258

    CAS  PubMed  Google Scholar 

  • Viterbo A, Wiest A, Brotman Y, Chet I, Kenerley C (2007) The 18mer peptaibols from Trichoderma virens elicit plant defence responses. Mol Plant Pathol 8:737–746

    CAS  PubMed  Google Scholar 

  • Walker TS, Bais HP, Halligan KM, Stermitz FR, Vivanco JR (2003) Metabolic profiling of root exudates of Arabidopsis thaliana. J Agric Food Chem 51:2548–2554

    CAS  PubMed  Google Scholar 

  • Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Huckelhoven R, Neumann C, von Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA 102:1386–13391

    Google Scholar 

  • Waller F, Mukherjee K, Deshmukh SD, Achatz B, Sharma M, Schaefer P, Kogel KH (2008) Systemic and local modulation of plant responses by Piriformospora indica and related Sebacinales species. J Plant Physiol 165:60–67

    CAS  PubMed  Google Scholar 

  • Woo S, Donzelli F, Scala F, Mach R, Harman G, Kubicek CP, Del Sorbo G, Lorito M (1999) Disruption of ech42 (endochitinase encoding) gene affects biocontrol activity in Trichoderma harzianum strain. Mol Plant-Microbe Interact 12:419–429

    CAS  Google Scholar 

  • Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4

    CAS  PubMed  Google Scholar 

  • Yedidia I, Benhamou N, Chet I (1999) Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl Environ Microbiol 65:1061–1070

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yedidia I, Benhamou N, Kapulnik Y, Chet I (2000) Induction and accumulation of PR proteins activity during early stages of root colonization by the mycoparasite Trichoderma harzianum strain T-203. Plant Physiol Biochem 38:863–873

    CAS  Google Scholar 

  • 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 69:7343–7353

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 68:60–66

    CAS  PubMed  Google Scholar 

  • Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Paré PW (2008) Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J 56:264–273

    CAS  PubMed  Google Scholar 

  • Zhang F, Yuan J, Yang X, Cui Y, Chen L, Ran W, Shen Q (2013) Putative Trichoderma harzianum mutant promotes cucumber growth by enhanced production of indole acetic acid and plant colonization. Plant Soil 368:433–444

    CAS  Google Scholar 

Download references

Acknowledgment

KB is grateful to BHU for the financial assistance. BKS, CK, and JSP are grateful to ICAR-AMAAS (project P-27/131) for providing financial support.

Author information

Authors and Affiliations

  1. Department of Mycology and Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, 221005, India

    Kartikay Bisen, Chetan Keswani, J. S. Patel, B. K. Sarma & H. B. Singh

Authors
  1. Kartikay Bisen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chetan Keswani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. S. Patel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. B. K. Sarma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. H. B. Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to H. B. Singh .

Editor information

Editors and Affiliations

  1. Amity Institute of Microbial Technology, Amity University, Noida, Uttar Pradesh, India

    Devendra K. Choudhary

  2. Amity Institute of Microbial Technology, Amity University, Noida, Uttar Pradesh, India

    Ajit Varma

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Science+Business Media Singapore

About this chapter

Cite this chapter

Bisen, K., Keswani, C., Patel, J.S., Sarma, B.K., Singh, H.B. (2016). Trichoderma spp.: Efficient Inducers of Systemic Resistance in Plants. In: Choudhary, D.K., Varma, A. (eds) Microbial-mediated Induced Systemic Resistance in Plants. Springer, Singapore. https://doi.org/10.1007/978-981-10-0388-2_12

Download citation

Publish with us

Policies and ethics

Search

Navigation