Non-target Effects of Trichoderma on Plants and Soil Microbial Communities

  • Monika Jangir
  • Satyawati Sharma
  • Shilpi SharmaEmail author


Biocontrol agents are currently considered as promising alternative to chemical fungicides because of the latter’s negative impacts on consumer health, plant health, and the environment. In the current biopesticide world, Trichoderma spp. has been globally accepted to prevent the invasion of pathogens, viz., Fusarium oxysporum, Verticillium dahliae, Pythium aphanidermatum, Rhizoctonia solani, etc. The antagonistic activity of Trichoderma spp. is attributed to several mechanisms, viz., mycoparasitism, antibiosis, induction of host systemic resistance, and production of hydrolytic enzymes. They not only have plant growth-promoting properties but also exert transient or long-term impact on the resident soil microbiome and may pose risk to beneficial non-target soil communities. Some compounds released by them in higher amount increase the sensitivity of the plant, and may pose negative impact on their growth. Additionally, Trichoderma spp. affects microbial community functions. The current chapter summarizes Trichoderma-pathogen-plant interaction, and the impact of Trichoderma spp. on plant growth, soil enzyme activities, and soil microbiome.


  1. Amaresan N, Kumar K, Venkadesaperuma G, Srivathsa NC (2018) Microbial community level physiological profiles of active mud volcano soils in Andaman and Nicobar Islands. Nat Acad Sci Lett 41:1–4CrossRefGoogle Scholar
  2. Araújo ASF, De Souza DG, De Almeida Lopes AC (2016) T-RFLP analysis of soil bacterial structure from Cerrado within the Sete Cidades National Park, Brazil. Neotrop Biodiversity 2:163–170CrossRefGoogle Scholar
  3. Blaya J, López-Mondéjar R, Lloret E, Pascual JA, Ros M (2013) Changes induced by Trichoderma harzianum in suppressive compost controlling Fusarium wilt. Pestic Biochem Physiol 107:112–119CrossRefGoogle Scholar
  4. Brimner TA, Boland GJ (2003) A review of the non-target effects of fungi used to biologically control plant diseases. Agric Ecosyst Environ 100:3–16CrossRefGoogle Scholar
  5. Chet I, Inbar J (1994) Biological control of fungal pathogens. Appl Biochem Biotechnol 48:37–43CrossRefGoogle Scholar
  6. Cook RJ, Bruckart WL, Coulson JR, Goettel MS, Humber RA, Lumsden RD, Maddox JV, McManus ML, Moore L, Meyer SF, Quimby PC Jr, Stack JP, Vaughn JL (1996) Safety of microorganisms intended for pest and plant disease control: a framework for scientific evaluation. Biol Control 7:335–351CrossRefGoogle Scholar
  7. Cordier C, Alabouvette C (2009) Effects of the introduction of a biocontrol strain of Trichoderma atroviride on non-target soil microorganisms. Eur J Soil Biol 7:267–274CrossRefGoogle Scholar
  8. Epelde L, Jauregi L, Urra J, Ibarretxe L, Romo J, Goikoetxea I, Garbisu C (2018) Characterization of composted organic amendments for agricultural use. Front Sustain Food Syst 2:Article 44CrossRefGoogle Scholar
  9. Frac M, Oszust K, Lipiec J (2012) Community level physiological profiles (CLPP), characterization and microbial activity of soil amended with dairy sewage sludge. Sensors 12:3253–3268CrossRefGoogle Scholar
  10. Garcia DE, Lopez BR, de-Bashan LE, Hirsch AM, Maymon M, Bashan Y (2018) Functional metabolic diversity of the bacterial community in undisturbed resource island soils in the southern Sonoran Desert. Land Degrad Dev 29:1467–1477CrossRefGoogle Scholar
  11. Gasoni L, Khan N, Yokoyama K, Chiessa GH, Kobayashi K (2008) Impact of Trichoderma harzianum biocontrol agent on functional diversity of soil microbial community in tobacco monoculture in Argentina. World J Agric Sci 4:527–532Google Scholar
  12. Goldman GH, Hayes C, Harman GE (1994) Molecular and cellular biology of biocontrol by Trichoderma spp. Trends Biotechnol 12:478–482CrossRefGoogle Scholar
  13. Gupta R, Mathimaran N, Wiemken A, Boller T, Bisaria VS, Sharma S (2014) Non-target effects of bioinoculants on rhizospheric microbial communities of Cajanus cajan. Appl Soil Ecol 76:26–33CrossRefGoogle Scholar
  14. Harman GE (2006) Overview of mechanisms and uses of Trichoderma spp. Phytopathology 96:190–194CrossRefGoogle Scholar
  15. Hashem A, Abd_Allah EF, Alqarawi AA, Al Huqail AA, Egamberdieva D (2014) Alleviation of abiotic salt stress in Ochradenus baccatus (Del.) by Trichoderma hamatum (Bonord.) Bainier. J Plant Interact 9:857–868CrossRefGoogle Scholar
  16. Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25CrossRefGoogle Scholar
  17. Howell CR (2006) Understanding the mechanisms employed by Trichoderma virens to effect biological control of cotton diseases. Phytopathology 96:178–180CrossRefGoogle Scholar
  18. Kleifeld O, Chet I (1992) Trichoderma harzianum interaction with plants and effect on growth response. Plant Soil 144:267–272CrossRefGoogle Scholar
  19. Kleyer H, Tecon R, Or D (2017) Resolving species level changes in a representative soil bacterial community using microfluidic quantitative PCR. Front Microbiol 8:Article 2017CrossRefGoogle Scholar
  20. Li S, Lü T, Zhang X, Gu G, Niu Y (2013) Effect of Trichoderma longbrachiatum T2 on functional diversity of cucumber rhizomicrobes. J Environ Biol 34:293–299PubMedGoogle Scholar
  21. Lladó S, Baldrian P (2017) Community-level physiological profiling analyses show potential to identify the copiotrophic bacteria present in soil environments. PLoS One 12:e0171638CrossRefGoogle Scholar
  22. Lorito M, Woo SL, Harman GE, Monte E (2010) Translational research on Trichoderma: from omics to the field. Annu Rev Phytopathol 48:395–417CrossRefGoogle Scholar
  23. Louis BP, Maron PA, Menasseri-Aubry S, Sarr A, Lévêque J, Mathieu O, Jolivet C, Leterme P, Viaud V (2016) Microbial diversity indexes can explain soil carbon dynamics as a function of carbon source. PLoS One 11:e0161251CrossRefGoogle Scholar
  24. Lumsden RD, Carter JP, Whipps JM, Lynch JM (1990) Comparison of biomass and viable propagule measurements in the antagonism of Trichoderma harzianum against Pythium ultimum. Soil Biol Biochem 22:187–194CrossRefGoogle Scholar
  25. McAllister CB, Garcia-Romera I, Godeas A, Ocampo JA (1994) In vitro interactions between Trichoderma koningii, Fusarium solani and Glomus mosseae. Soil Biol Biochem 26:1369–1374CrossRefGoogle Scholar
  26. McLean KL, Dodd SL, Minchin RF, Ohkura M, Bienkowski D, Stewart A (2014) Non-target impacts of the biocontrol agent Trichoderma atroviride on plant health and soil microbial communities in two native ecosystems in New Zealand. Australas Plant Pathol 43:33–45CrossRefGoogle Scholar
  27. Morán-Diez E, Rubio B, Domínguez S, Hermosa R, Monte E, Nicolás C (2012) Transcriptomic response of Arabidopsis thaliana after 24 h incubation with the biocontrol fungus Trichoderma harzianum. J Plant Physiol 169:614–620CrossRefGoogle Scholar
  28. Mukherjee M, Mukherjee PK, Horwitz BA, Zachow C, Berg G, Zeilinger S (2012) Trichoderma–plant–pathogen interactions: advances in genetics of biological control. Indian J Microbiol 52:522–529CrossRefGoogle Scholar
  29. Naseby DC, Lynch JM (1998) Impact of wild-type and genetically modified Pseudomonas fluorescens on soil enzyme activities and microbial population structure in the rhizosphere of pea. Mol Ecol 7:617–625CrossRefGoogle Scholar
  30. Naseby DC, Pascual JA, Lynch JM (2000) Effect of biocontrol strains of Trichoderma on plant growth, Pythium ultimum populations, soil microbial communities and soil enzyme activities. J Appl Microbiol 88:161–169CrossRefGoogle Scholar
  31. Nieto-Jacobo MF, Steyaert JM, Salazar-Badillo FB, Nguyen DV, Rostás M, Braithwaite M, De Souza JT, Bremont JFJ, Ohkura M, Stewart A, Mendoza-Mendoza A (2017) Environmental growth conditions of Trichoderma spp. affects indole acetic acid derivatives, volatile organic compounds, and plant growth promotion. Front Plant Sci 8:Article 102CrossRefGoogle Scholar
  32. Ondreičková K, Piliarová M, Bušo R, Hašana R, Schreiber Ľ, Gubiš J, Kraic J (2018) The structure and diversity of bacterial communities in differently managed soils studied by molecular fingerprinting methods. Sustainability 10:1095–1111CrossRefGoogle Scholar
  33. Pacwa-Płociniczak M, Płociniczak T, Yu D, Kurola JM, Sinkkonen A, Piotrowska-Seget Z, Romantschuk M (2018) Effect of Silene vulgaris and heavy metal pollution on soil microbial diversity in long-term contaminated soil. Water Air Soil Pollut 229:1–13CrossRefGoogle Scholar
  34. Pang G, Cai F, Li R, Zhao Z, Li R, Gu X, Shen Q, Chen W (2017) Trichoderma-enriched organic fertilizer can mitigate microbiome degeneration of monocropped soil to maintain better plant growth. Plant Soil 416:181–192CrossRefGoogle Scholar
  35. Pascual J, Blanco S, Ramos JL, Van Dillewijn P (2018) Responses of bulk and rhizosphere soil microbial communities to thermoclimatic changes in a Mediterranean ecosystem. Soil Biol Biochem 118:130–144CrossRefGoogle Scholar
  36. Peñuelas J, Filella I (1998) Visible and near-infrared reflectance techniques for diagnosing plant physiological status. Trends Plant Sci 3:151–156CrossRefGoogle Scholar
  37. Ros M, Raut I, Santisima-Trinidad AB, Pascual JA (2017) Relationship of microbial communities and suppressiveness of Trichoderma fortified composts for pepper seedlings infected by Phytophthora nicotianae. PLoS One 12:e0174069CrossRefGoogle Scholar
  38. Sampson PH, Zarco-Tejada PJ, Mohammed GH, Miller JR, Noland TL (2003) Hyperspectral remote sensing of forest condition: estimating chlorophyll content in tolerant hardwoods. For Sci 49:381–391Google Scholar
  39. Saravanakumar K, Li Y, Yu C, Wang QQ, Wang M, Sun J, Gao JX, Chen J (2017) Effect of Trichoderma harzianum on maize rhizosphere microbiome and biocontrol of Fusarium stalk rot. Sci Rep 7:1771–1783CrossRefGoogle Scholar
  40. Shi WL, Chen XL, Wang LX, Gong ZT, Li S, Li CL, Xie BB, Zhang W, Shi M, Li C, Zhang YZ, Song XY (2016) Cellular and molecular insight into the inhibition of primary root growth of Arabidopsis induced by peptaibols, a class of linear peptide antibiotics mainly produced by Trichoderma spp. J Exp Bot 67:2191–2205CrossRefGoogle Scholar
  41. 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 147:2147–2163CrossRefGoogle Scholar
  42. Shrivastava S, Prasad R, Varma A (2014) Anatomy of root from eyes of a microbiologist. In: Morte A, Varma A (eds) Root engineering, vol 40. Springer, Berlin, pp 3–22CrossRefGoogle Scholar
  43. Soliman T, Yang SY, Yamazaki T, Jenke-Kodama H (2017) Profiling soil microbial communities with next-generation sequencing: the influence of DNA kit selection and technician technical expertise. Peer J 5:e4178CrossRefGoogle Scholar
  44. Szczepaniak Z, Cyplik P, Juzwa W, Czarny J, Staninska J, Piotrowska-Cyplik A (2015) Antibacterial effect of the Trichoderma viride fungi on soil microbiome during PAH’s biodegradation. Int Biodeterior Biodegrad 104:170–177CrossRefGoogle Scholar
  45. Trabelsi D, Mhamdi R (2013) Microbial inoculants and their impact on soil microbial communities: a review. Biomed Res Int 2013:Article ID 863240CrossRefGoogle Scholar
  46. Umadevi P, Anandaraj M, Srivastav V, Benjamin S (2018) Trichoderma harzianum MTCC 5179 impacts the population and functional dynamics of microbial community in the rhizosphere of black pepper (Piper nigrum L.). Braz J Microbiol 49(3):463–470. CrossRefPubMedGoogle Scholar
  47. Vázquez MM, César S, Azcón R, Barea JM (2000) Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Appl Soil Ecol 15:261–272CrossRefGoogle Scholar
  48. Verma M, Brar SK, Tyagi RD, Surampalli RY, Valero JR (2007) Antagonistic fungi, Trichoderma spp.: panoply of biological control. Biochem Eng J 37:1–20CrossRefGoogle Scholar
  49. Wang S, Chen X, Gong H, Cai Z (2018) Response of soil microbial abundance and diversity in Sacha Inchi (Plukenetia volubilis L.) farms with different land-use histories in a tropical area of Southwestern China. Arch Agron Soil Sci 64:588–596CrossRefGoogle Scholar
  50. Wood JL, Zhang C, Mathews ER, Tang C, Franks AE (2016) Microbial community dynamics in the rhizosphere of a cadmium hyper-accumulator. Sci Rep 6:36067CrossRefGoogle Scholar
  51. Wu Z, Lin W, Li B, Wu L, Fang C, Zhang Z (2015) Terminal restriction fragment length polymorphism analysis of soil bacterial communities under different vegetation types in subtropical area. PLoS One 10:e0129397CrossRefGoogle Scholar
  52. Zhang Z, Qu Y, Li S, Feng K, Wang S, Cai W, Liang Y, Li H, Xu M, Yin H, Deng Y (2017) Soil bacterial quantification approaches coupling with relative abundances reflecting the changes of taxa. Sci Rep 7:4837CrossRefGoogle Scholar
  53. Zhu S, Wang Y, Xu X, Liu T, Wu D, Zheng X, Tang S, Dai Q (2018) Potential use of high-throughput sequencing of soil microbial communities for estimating the adverse effects of continuous cropping on ramie (Boehmeria nivea L. Gaud). PLoS One 13:e0197095CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Monika Jangir
    • 1
  • Satyawati Sharma
    • 1
  • Shilpi Sharma
    • 2
    Email author
  1. 1.Centre for Rural Development and TechnologyIndian Institute of Technology DelhiNew DelhiIndia
  2. 2.Department of Biochemical Engineering and BiotechnologyIndian Institute of Technology DelhiNew DelhiIndia

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