Toward an Integrated Resource Management: Harnessing Trichoderma for Sustainable Intensification in Agriculture

  • Sumita PalEmail author
  • H. B. Singh
  • Deep Ranjan Sarkar
  • Ranjeet Singh Yadav
  • Amitava Rakshit


Trichoderma has proved its diverse role in agriculture as an efficient microorganism to overcome numerous challenges associated with it. Being ubiquitous in nature, studies conducted on it are totally safe and involve low-cost implementation. Initially the research works highlighted this microbe as a suitable biocontrol agent against most phytopathogens. Many strains of Trichoderma have been successfully screened out for its beneficial effects on soil fertility and plant health aspects, but we need an environment which is free of pollution, and therefore focusing on multiple functions of Trichoderma to fight against various biotic and abiotic stresses and the hazardous pollutants which can affect our food chain is important to maintain sustainability. This mini review attempts to include the potentials of Trichoderma in present and upcoming condition of resource management.


Abiotic and biotic stress Tolerance Plant growth promotion Trichoderma 



The first author thanks the Department of Science and Technology, New Delhi, for the award of Woman Scientist Scheme (SR/WOS-A/LS-1199/2015) during the course of study.


  1. Abd El-Baki G, Mostafa D (2014) The potentiality of Trichoderma harzianum in alleviation the adverse effects of salinity in faba bean plants. Acta Biol Hung 65(4):451–468CrossRefPubMedGoogle Scholar
  2. Abd-El-Khair H, Khalifa RKM, Haggag KHE (2010) Effect of Trichoderma species on damping off diseases incidence, some plant enzymes activity and nutritional status of bean plants. J Am Sci 6(9):486–497Google Scholar
  3. Abdullah MT, Ali NY, Suleman P (2008) Biological control of Sclerotinia sclerotiorum (Lib.) de Bary with Trichoderma harzianum and Bacillus amyloliquefaciens. Crop Prot 27(10):1354–1359CrossRefGoogle Scholar
  4. Argumedo-Delira R, Alarcón A, Ferrera-Cerrato R, Almaraz JJ, Peña-Cabriales JJ (2012) Tolerance and growth of 11 Trichoderma strains to crude oil, naphthalene, phenanthrene and benzo [a] pyrene. J Environ Manag 95:S291–S299CrossRefGoogle Scholar
  5. Arriagada C, Aranda E, Sampedro I, Garcia-Romera I, Ocampo JA (2009) Contribution of the saprobic fungi Trametes versicolor and Trichoderma harzianum and the arbuscular mycorrhizal fungi Glomus deserticola and G. claroideum to arsenic tolerance of Eucalyptus globulus. Bioresour Technol 100(24):6250–6257CrossRefPubMedGoogle Scholar
  6. Azad K, Kaminskyj S (2016) A fungal endophyte strategy for mitigating the effect of salt and drought stress on plant growth. Symbiosis 68(1–3):73–78CrossRefGoogle Scholar
  7. Azarmi R, Hajieghrari B, Giglou A (2011) Effect of Trichoderma isolates on tomato seedling growth response and nutrient uptake. Afr J Biotechnol 10(31):5850–5855Google Scholar
  8. Bae H, Sicher RC, Kim MS, Kim SH, Strem MD, Melnick RL, Bailey BA (2009) The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J Exp Bot 60(11):3279–3295CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bailey BA, Lumsden RD (1998) Direct effects of Trichoderma and Gliocladium on plant growth and resistance to pathogens. In: Kubicek CP, Harman GE, Ondik KL (eds) Trichoderma and Gliocladium: enzymes, biological control and commercial applications. Taylor and Francis, London, pp 185–204Google Scholar
  10. Benítez T, Rincón AM, Limón MC, Codón AC (2004) Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7(4):249–260PubMedGoogle Scholar
  11. Bigirimana J, De Meyer G, Poppe J, Elad Y, Höfte M (1997) Induction of systemic resistance on bean (Phaseolus vulgaris) by Trichoderma harzianum. Mededelingen Van De Faculteit Landbouwkundige En Toegepaste Biologische Wetenschappen, Universiteit Gent 62:1001–1007Google Scholar
  12. 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(2):779–789CrossRefPubMedPubMedCentralGoogle Scholar
  13. Cao L, Jiang M, Zeng Z, Du A, Tan H, Liu Y (2008) Trichoderma atroviride F6 improves phytoextraction efficiency of mustard (Brassica juncea (L.) Coss. var. foliosa Bailey) in Cd, Ni contaminated soils. Chemosphere 71(9):1769–1773CrossRefPubMedGoogle Scholar
  14. Chet I, Inbar J (1994) Biological control of fungal pathogens. Appl Biochem Biotechnol 48:37–43CrossRefPubMedGoogle Scholar
  15. Delgado-Jarana J, Moreno-Mateos MÁ, Benítez T (2003) Glucose uptake in Trichoderma harzianum: role of gtt1. Eukaryot Cell 2(4):708–717CrossRefPubMedPubMedCentralGoogle Scholar
  16. Dixit P, Mukherjee PK, Ramachandran V, Eapen S (2011) Glutathione transferase from Trichoderma virens enhances cadmium tolerance without enhancing its accumulation in transgenic Nicotiana tabacum. PLoS One 6(1):e16360CrossRefPubMedPubMedCentralGoogle Scholar
  17. 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(10):749–759CrossRefPubMedGoogle Scholar
  18. El-Mohamedy RS, Shafeek MR, Fatma AR (2015) Management of root rot diseases and improvement growth and yield of green bean plants using plant resistance inducers and biological seed treatments. J Agric Technol 11(5):1219–1234Google Scholar
  19. Errasquın EL, Vazquez C (2003) Tolerance and uptake of heavy metals by Trichoderma atroviride isolated from sludge. Chemosphere 50(1):137–143CrossRefGoogle Scholar
  20. Ezzi MI, Lynch JM (2005) Plant microcosm studies demonstrating bioremediation of cyanide toxicity by Trichoderma and Fusarium spp. Biol Fertil Soils 42(1):40–44CrossRefGoogle Scholar
  21. Friedl MA, Schmoll M, Kubicek CP, Druzhinina IS (2008) Photostimulation of Hypocrea atroviridis growth occurs due to a cross-talk of carbon metabolism, blue light receptors and response to oxidative stress. Microbiology 154(4):1229–1241CrossRefPubMedGoogle Scholar
  22. 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(4):133–142Google Scholar
  23. Guler NS, Pehlivan N, Karaoglu SA, Guzel S, Bozdeveci A (2016) Trichoderma atroviride ID20G inoculation ameliorates drought stress-induced damages by improving antioxidant defence in maize seedlings. Acta Physiol Plant 38(6):1–9CrossRefGoogle Scholar
  24. Harman GE (2000) Myths and dogmas of biocontrol changes in perceptions derived from research on Trichoderma harzianum T-22. Plant Dis 84(4):377–393CrossRefGoogle Scholar
  25. Harman GE (2006) Overview of mechanisms and uses of Trichoderma spp. Phytopathology 96(2):190–194CrossRefPubMedGoogle Scholar
  26. Harman GE, Mastouri F (2010) Enhancing nitrogen use efficiency in wheat using Trichoderma seed inoculants, vol 7. International Society for Plant-Microbe Interactions, St. Paul, pp 1–4Google Scholar
  27. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species-opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2(1):43–56CrossRefPubMedGoogle Scholar
  28. Herrera-Estrella A, Chet I (2004) The biological control agent Trichoderma: from fundamentals to applications. In: Arora D (ed) Handbook of fungal biotechnology. Dekker, New York, pp 2,147–2,156Google Scholar
  29. Howell CR (2002) Cotton seedling preemergence damping-off incited by Rhizopus oryzae and Pythium spp. and its biological control with Trichoderma spp. Phytopathology 92(2):177–180CrossRefPubMedGoogle Scholar
  30. Jaklitsch WM (2009) European species of Hypocrea Part I. The green-spored species. Stud Mycol 63:1–91CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kredics L, Antal Z, Manczinger L, Nagy E (2001) Breeding of mycoparasitic Trichoderma strains for heavy metal resistance. Lett Appl Microbiol 33(2):112–116CrossRefPubMedGoogle Scholar
  32. Kubicek CP, Mikus M, Schuster A, Schmoll M, Seiboth B (2009) Metabolic engineering strategies for the improvement of cellulase production by Hypocrea jecorina. Biotechnol Biofuels 2(1):1CrossRefGoogle Scholar
  33. Kubicek CP, Herrera-Estrella A, Seidl-Seiboth V, Martinez DA, Druzhinina IS, Thon M, Zeilinger S, Casas-Flores S, Horwitz BA, Mukherjee PK, Mukherjee M (2011) Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol 12(4):1CrossRefGoogle Scholar
  34. Lorito M, Woo SL, Harman GE, Monte E (2010) Translational research on Trichoderma: from’omics to the field. Annu Rev Phytopathol 48:395–417CrossRefPubMedGoogle Scholar
  35. Lynch JM, Moffat AJ (2005) Bioremediation–prospects for the future application of innovative applied biological research. Ann Appl Biol 146(2):217–221CrossRefGoogle Scholar
  36. Mastouri F, Björkman T, Harman GE (2010) Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology 100(11):1213–1221CrossRefPubMedGoogle Scholar
  37. Mishra A, Nautiyal CS (2009) Functional diversity of the microbial community in the rhizosphere of chickpea grown in diesel fuel-spiked soil amended with Trichoderma reesei using sole-carbon-source utilization profiles. World J Microbiol Biotechnol 25(7):1175–1180CrossRefGoogle Scholar
  38. Miyadera H, Shiomi K, Ui H, Yamaguchi Y, Masuma R, Tomoda H, Osanai A, Kita K, Ōmura S (2003) Atpenins, potent and specific inhibitors of mitochondrial complex II (succinate-ubiquinone oxidoreductase). Proc Natl Acad Sci 100(2):473–477CrossRefPubMedPubMedCentralGoogle Scholar
  39. Mohammadi K, Ghalavand A, Aghaalikhani M (2010) Effect of organic matter and biofertilizers on chickpea quality and biological nitrogen fixation. World Acad Sci, Eng Tech 68:1144–1149Google Scholar
  40. Montero-Barrientos M, Hermosa R, Cardoza RE, Gutiérrez S, Monte E (2011) Functional analysis of the Trichoderma harzianum nox1 gene, encoding an NADPH oxidase, relates production of reactive oxygen species to specific biocontrol activity against Pythium ultimum. Appl Environ Microbiol 77(9):3009–3016CrossRefPubMedPubMedCentralGoogle Scholar
  41. Mudawi HI, Idris MO (2015) Efficacy of the bioagents Bacillus isolates and Trichoderma spp. in the control of wilt/root-rot disease in chickpea. World J Sci Technol Sustain Dev 12(4):303–314CrossRefGoogle Scholar
  42. Mukherjee I, Gopal M (1996) Degradation of chlorpyrifos by two soil fungi Aspergillus niger and Trichoderma viride. Toxicol Environ Chem 57(1–4):145–151CrossRefGoogle Scholar
  43. Mukherjee PK, Horwitz BA, Herrera-Estrella A, Schmoll M, Kenerley CM (2013) Trichoderma research in the genome era. Annu Rev Phytopathol 51:105–129CrossRefPubMedGoogle Scholar
  44. Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moënne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321(1–2):341–361CrossRefGoogle Scholar
  45. Rawat L, Singh Y, Shukla N, Kumar J (2012) Seed biopriming with salinity tolerant isolates of Trichoderma harzianum alleviates salt stress in rice: growth, physiological and biochemical characteristics. J Plant Pathology 94(2):353–365Google Scholar
  46. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim YO, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2(4):404–416CrossRefPubMedGoogle Scholar
  47. Sallenave C, Pouchus YF, Bardouil M, Lassus P, Roquebert MF, Verbist JF (1999) Bioaccumulation of mycotoxins by shellfish: contamination of mussels by metabolites of a Trichoderma koningii strain isolated in the marine environment. Toxicon 37(1):77–83CrossRefPubMedGoogle Scholar
  48. Saloheimo M, Paloheimo M, Hakola S, Pere J, Swanson B, Nyyssönen E, Bhatia A, Ward M, Penttilä M (2002) Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials. Eur J Biochem 269(17):4202–4211CrossRefPubMedGoogle Scholar
  49. Saravanakumar K, Arasu VS, Kathiresan K (2013) Effect of Trichoderma on soil phosphate solubilization and growth improvement of Avicennia marina. Aquat Bot 104:101–105CrossRefGoogle Scholar
  50. Saxena A, Raghuwanshi R, Singh HB (2016) Elevation of defense network in chilli against Colletotrichum capsici by Phyllospheric Trichoderma strain. J Plant Growth Regul 35(2):377–389CrossRefGoogle Scholar
  51. Schmoll M, Franchi L, Kubicek CP (2005) Envoy, a PAS/LOV domain protein of Hypocrea jecorina (Anamorph Trichoderma reesei), modulates cellulase gene transcription in response to light. Eukaryot Cell 4(12):1998–2007CrossRefPubMedPubMedCentralGoogle Scholar
  52. Schuster A, Schmoll M (2010) Biology and biotechnology of Trichoderma. Appl Microbiol Biotechnol 87(3):787–799CrossRefPubMedPubMedCentralGoogle Scholar
  53. Shoresh M, Harman GE (2008) The molecular basis of shoot responses of maize seedlings to Trichoderma harzianum T22 inoculation of the root: a proteomic approach. Plant Physiol 147(4):2147–2163CrossRefPubMedPubMedCentralGoogle Scholar
  54. Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43CrossRefPubMedGoogle Scholar
  55. Singh SP, Singh HB, Singh DK, Rakshit A (2014) Trichoderma-mediated enhancement of nutrient uptake and reduction in incidence of Rhizoctonia solani in tomato. Egypt J Biol 16(1):29–38CrossRefGoogle Scholar
  56. Sreerama L, Veerabhadrappa PS (1993) Isolation and properties of carboxylesterases of the termite gut-associated fungus, Xylaria nigripes. K., and their identity from the host termite, Odentotermes horni. W., mid-gut carboxylesterases. Int J Biochem 25(11):1637–1651CrossRefPubMedGoogle Scholar
  57. Urík M, Čerňanský S, Ševc J, Šimonovičová A, Littera P (2007) Biovolatilization of arsenic by different fungal strains. Water Air Soil Pollut 186(1–4):337–342CrossRefGoogle Scholar
  58. 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(2):792–808CrossRefPubMedPubMedCentralGoogle Scholar
  59. Velázquez-Robledo R, Contreras-Cornejo HA, Macías-Rodríguez L, Hernández-Morales A, Aguirre J, Casas-Flores S, López-Bucio J, Herrera-Estrella A (2011) Role of the 4-phosphopantetheinyl transferase of Trichoderma virens in secondary metabolism and induction of plant defense responses. Mol Plant-Microbe Interact 24(12):1459–1471CrossRefPubMedGoogle Scholar
  60. Vey A, Hoagland RE, Butt TM (2001) Toxic metabolites of fungal biocontrol agents. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems and potential. CABI, Bristol, pp 311–346CrossRefGoogle Scholar
  61. Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Woo SL, Lorito M (2008) Trichoderma–plant–pathogen interactions. Soil Biol Biochem 40(1):1–10CrossRefGoogle Scholar
  62. 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(1):151–158PubMedGoogle Scholar
  63. Wiest A, Grzegorski D, Xu BW, Goulard C, Rebuffat S, Ebbole DJ, Bodo B, Kenerley C (2002) Identification of peptaibols from Trichoderma virens and cloning of a peptaibol synthetase. J Biol Chem 277(23):20862–20868CrossRefPubMedGoogle Scholar
  64. 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(3):1061–1070PubMedPubMedCentralGoogle Scholar
  65. 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(12):7343–7353CrossRefPubMedPubMedCentralGoogle Scholar
  66. Yoder AJ, Christensen BS, Croxall TJ, Tank JL, Sammataro D (2008) Suppression of growth rate of colony-associated fungi by high fructose corn syrup feeding supplement, formic acid, and oxalic acid. J Apicult Res Bee World 47(2):126–130Google Scholar
  67. 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(2):131–140CrossRefPubMedGoogle Scholar
  68. Zeng X, Su S, Jiang X, Li L, Bai L, Zhang Y (2010) Capability of pentavalent arsenic bioaccumulation and biovolatilization of three fungal strains under laboratory conditions. CLEAN–Soil Air Water 38(3):238–241CrossRefGoogle Scholar
  69. Zhou X, Xu S, Liu L, Chen J (2007) Degradation of cyanide by Trichoderma mutants constructed by restriction enzyme mediated integration (REMI). Bioresour Technol 98(15):2958–2962CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Sumita Pal
    • 1
    Email author
  • H. B. Singh
    • 1
  • Deep Ranjan Sarkar
    • 2
  • Ranjeet Singh Yadav
    • 2
  • Amitava Rakshit
    • 2
  1. 1.Department of Mycology and Plant PathologyInstitute of Agricultural Science, BHUVaranasiIndia
  2. 2.Department of Soil Science and Agricultural ChemistryInstitute of Agricultural Science, BHUVaranasiIndia

Personalised recommendations