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Trichoderma pp 167-185 | Cite as

TrichodermaFusarium Interactions: A Biocontrol Strategy to Manage Wilt

  • Ishwar Prakash Sharma
  • Anil K. Sharma
Chapter
  • 60 Downloads
Part of the Rhizosphere Biology book series (RHBIO)

Abstract

Soil-borne microorganisms are either beneficial or harmful to proper plant growth and crop yield. All these microorganisms share the same niche in the rhizosphere and interact with each other. Fusarium is one of the most important fungal pathogen in the soil, which is found nearly in every agricultural crop and causes yield loss due to suppression in plant growth and development. Various chemical methods are being used for its management, which are expensive and hazardous to the environment for sustainable development due to their toxicity. Biological control is one of the most effective and popular ways to manage it because it has very low level of toxicity in the environmental point of view and is cost-effective. Among the biocontrol agents, Trichoderma is a popular symbiotic fungus that inhibits or controls the Fusarium wilt through the mechanism of mycoparasitism, completion, production of various lytic enzymes, and other antimicrobial activities along with enhancement in the growth of the host plant by the production of plant growth hormones. In the soil, Trichoderma releases various antimycoparasitic proteins, enzymes, volatile and nonvolatile compounds, and other secondary metabolites that have the potency to solubilize nutrients and defend against pathogens. Due to these qualities, Trichoderma enhances growth in plants and protect them from soil pathogenic microorganisms. A mechanism from hyphal attraction to cell lysis via attachment and coiling performed in a series in the interaction of Trichoderma and Fusarium. Thus Trichoderma induces systemic resistance in the host plant due to pathogen inhibition and would be a potent biocontrol agent to attain sustainable agriculture, for better growth, production, and yield.

Keywords

Biocontrol Fusarium Metabolites Sustainable Trichoderma 

References

  1. Abdelrahman M, Abdel-Motaal F, El-Saved M, Jogaiah S, Shigyo M, Ito S, Tran LS (2016) Dissection of Trichoderma longibrachiatum-induced defense in onion (Allium cepa L.) against Fusarium oxysporum f. Sp. cepa by target metabolite profiling. Plant Sci 245:128–138CrossRefGoogle Scholar
  2. Adhikary MC, Begum HA, Meah MB (2017) Possibility of recovering Fusarium wilt affected eggplants by Trichoderma. Int J Agric Res Innov Technol 7(1):38–42CrossRefGoogle Scholar
  3. Adie BAT, Perez-Perez J, Perez-Perez MM et al (2007) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19:1665–1681PubMedPubMedCentralCrossRefGoogle Scholar
  4. Akrami M, Golzary H, Ahmadzadeh M (2011) Evaluation of different combinations of Trichoderma species for controlling Fusarum rot of lentil. Afr J Biotechnol 10:2653–2658CrossRefGoogle Scholar
  5. Althaf HSK, Srinivas P (2013) Association of arbuscular mycorrhizal fungi and other rhizosphere microbes with different medicinal plants. Res J Biotechnol 8(6):24–28Google Scholar
  6. Altinok HH, Erdogan O (2015) Determination of the in vitro effect of Trichoderma harzianum on phytopathogenic strains of Fusarium oxysporum. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 43(2):494–500CrossRefGoogle Scholar
  7. Al-Tuwaijiri MMY (2008) Biological control of Fusarium root-rot of cucumber (Cucumis sativus L.) by rhizospheric isolates of Bacillus subtilis and Trichoderma viride. Egypt J Exp Biol (Bot) 4:79–86Google Scholar
  8. Al-Tuwaijri MMY (2009) Role of the bio-control agents, Trichoderma viride and Bacillus subtilis, in elimination of the deteriorative effects of the root-rot pathogens, Fusarium oxysporum and F. Solani, on some metabolic and enzyme activities of cucumber plants. Egypt J Exp Biol (Bot) 5:29–35Google Scholar
  9. 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 60:3279–3295PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bailey BA, Stream MD, Wood D (2009) Trichoderma species form endophytic associations within Theobroma cacao trichomes. Mycol Res 113:1365–1376CrossRefPubMedGoogle Scholar
  11. Bari R, Jones JDG (2009) Role of plant hormones in plant defense responses. Plant Mol Biol 69:473–488PubMedCrossRefGoogle Scholar
  12. Berges MSL, Hera C, Sulyok M, Schafer K, Capilla J, Guarro J, Di Pietro A (2013) The velvet complex governs mycotoxin production and virulence of Fusarium oxysporum on plant and mammalian hosts. Mol Microbiol 86(1):49–65CrossRefGoogle Scholar
  13. Boughalleb-M’Hamdi N, Salem IB, M’Hamdi M (2018) Evaluation of the efficiency of Trichoderma, Penicillium, and Aspergillus species as biological control agents against four soil-borne fungi of melon and watermelon. Egypt J Biol Pest Cont 28:25.  https://doi.org/10.1186/s41938-017-0010-3CrossRefGoogle Scholar
  14. Brotman Y, Lisec J, Meret M, Chet I, Willmitzer L, Viterbo A (2012) Transcript and metabolite analysis of the Trichoderma induced systemic resistance response to Pseudomonas syringe in Arabidopsis thaliana. Microbiology 158:139–146PubMedPubMedCentralCrossRefGoogle Scholar
  15. Cargnello M, Roux PP (2011) Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol Mol Biol Rev 75(1):50–83PubMedPubMedCentralCrossRefGoogle Scholar
  16. Carvalho DDC, Junior ML, Martins I, Inglis PW, Mello SCM (2014) Biological control of Fusarium oxysporum f. sp. phaseoli by Trichoderma harzianum and its use of common bean seed treatment. Trop Plant Pathol 39(5):384–391CrossRefGoogle Scholar
  17. Castillo AG, Puig CG, Cumagun CJR (2019) Non-synergistic effect of Trichoderma harzianum and Glomus spp. in reducing infection of Fusarium wilt in banana. Pathogens 8.  https://doi.org/10.3390/pathogens8020043
  18. Catalano V, Vergara M, Hauzenberger JR et al (2011) Use of a nonhomologous end-joining-deficient strain (delta-ku70) of the biocontrol fungus Trichoderma virens to investigate the function of the laccase gene lcc1 in sclerotia degradation. Curr Genet 57:13–23PubMedCrossRefGoogle Scholar
  19. Chaves NP, Staver C, Dita A (2016) Potential of Trichoderma asperellum for biocontrol of Fusarium wilt in banana. Acta Hort 1114:261–266CrossRefGoogle Scholar
  20. Chen LJ, Sun SZ, Miao CP, Wu K, Chen YW, Xu LH, Guan HL, Zhao LX (2015) Endophytic Trichoderma gamsii YIM PH30019: a promising biocontrol agent with hyperosmolar, mycoparasitism and antagonistic activities of induced volatile organic compounds on root-rot pathogenic fungi of Panax notoginseng. J Ginseng Res 38:1–10Google Scholar
  21. Cherkupally C, Amballa H, Reddy BN (2017) In vitro antagonistic activity of Trichoderma species against Fusarium oxysporum f. sp. melongenae. Int J Appl Agric Res 12(1):87–95Google Scholar
  22. Choudhary S, Reena M (2012) In-vitro antagonism of indigenous Trichoderma isolates against phytopathogen causing wilt of lentil. Int J Life Sci Pharma Res 2(3):195–202Google Scholar
  23. Christopher DJ, Raj TS, Rani SU, Udhayakumar R (2010) Role of defense enzymes activity in tomato as induced by Trichoderma virens against Fusarium wilt caused by Fusarium oxysporum f sp. lycopersici. J Biopest 3:158–162Google Scholar
  24. Contreras-Cornejo H, Macias-Rodriguez L, Cortes-Penagos C, Lopez-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
  25. Contreras-Cornejo HA, Macias-Rodriguez 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(4):1–17CrossRefGoogle Scholar
  26. Coral OEC, Criollo MT, Vallejo JD (2017) Antagonism of Trichoderma spp. strains against pea (Pisum sativum L.) Fusarium wilt caused by Fusarium oxysporum f. sp. pisi. Acta Agron 66(3):442–448CrossRefGoogle Scholar
  27. Cornejo HAC, Rodriguez LM, Vergara AG, Bucio JL (2015) Trichoderma modulates stomatal aperture and leaf transpiration through an abscisic acid-dependent mechanism in Arabidopsis. J Plant Growth Regul 34(2):425–434CrossRefGoogle Scholar
  28. Daami-Remadi M, Hibar K, Jabnoun-Khiareddine H, Ayed F, El Mahjoub M (2006) Effect of two Trichoderma species on severity of potato tuber dry rot caused by Tunisian Fusarium complex. Int J Agric Res 1:432–441CrossRefGoogle Scholar
  29. Dabire TG, Bonzi S, Somda I, Legreve A (2016) Evaluation of the potential of Trichoderma harzianum as a plant growth promoter and biocontrol agent against Fusarium damping-off in onion in Burkina Faso. Asian J Plant Pathol 10:49–60CrossRefGoogle Scholar
  30. Dehariya K, Shukla A, Sheikh IA, Vyas D (2015) Trichoderma and arbuscular mycorrhizal fungi based biocontrol of Fusarium udum butler and their growth promotion effects on pigeon pea. J Agric Sci Technol 17:505–517Google Scholar
  31. Dinolfo MI, Castanares E, Stenglei SA (2017) Fusarium–plant interaction: state of the art - a review. Plant Protect Sci 53(2):61–70CrossRefGoogle Scholar
  32. Djonovic S, Pozo MJ, Kenerley CM (2006) Tvbgn3, a beta-1,6-glucanase from the biocontrol fungus Trichoderma virens, is involved in mycoparasitism and control of Pythium ultimum. Appl Environ Microbiol 72:7661–7670PubMedPubMedCentralCrossRefGoogle Scholar
  33. 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 145:875–889PubMedPubMedCentralCrossRefGoogle Scholar
  34. Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A et al (2011) Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9:749–759PubMedPubMedCentralCrossRefGoogle Scholar
  35. Druzhinina IS, Shelest E, Kubicek CP (2012) Novel traits of Trichoderma predicted through the analysis of its secretome. FEMS Microbiol Lett 337:1.  https://doi.org/10.1111/j.1574-6968.2012.02665.xCrossRefPubMedPubMedCentralGoogle Scholar
  36. Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209PubMedCrossRefGoogle Scholar
  37. El-Hasan A, Walker F, Buchenauer H (2008) Trichoderma harzianum and its metabolite 6-pentyl-alpha-pyrone suppress fusaric acid produced by Fusarium moniliforme. J Phytopathol 156:79–87CrossRefGoogle Scholar
  38. 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 125:369–377PubMedPubMedCentralCrossRefGoogle Scholar
  39. Gawehns F, Houterman PM, Ichou FA et al (2013) The Fusarium oxysporum effector six6 contributes to virulence and suppresses i-2-mediated cell death. Mol Plant-Microbe Interact 27(4):336–348CrossRefGoogle Scholar
  40. Ghanbarzadeh B, Safaie N, Goltapeh EM (2014) Antagonistic activity and hyphal interactions of Trichoderma spp. against Fusarium proliferatum and F. oxysporum in vitro. Arch Phytopathol Plant Protect 47(16):197–198CrossRefGoogle Scholar
  41. Giurgiu RM, Dumitras A, Morar G, Scheewe P, Schroder FG (2018) A study on the biological control of Fusarium oxysporum using Trichoderma spp., on soil and rockwool substrates in controlled environment. Not Bot Horti Agrobo 46(1):260–269CrossRefGoogle Scholar
  42. Gruber S, Zeilinger S (2014) The transcription factor ste12 mediates the regulatory role of the tmk1 map kinase in mycoparasitism and vegetative hyphal fusion in the filamentous fungus Trichoderma atroviride. PLoS One 9(10):e111636.  https://doi.org/10.1371/journal.pone.0111636CrossRefPubMedPubMedCentralGoogle Scholar
  43. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species - opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56PubMedPubMedCentralCrossRefGoogle Scholar
  44. Howell CR (2006) Understanding the mechanisms employed by Trichoderma virens to effect biological control of cotton diseases. Phytopathology 96:178–180PubMedCrossRefGoogle Scholar
  45. Jogaiah S, Abdelrahman M, Tran LP, Ito SI (2018) Different mechanisms of Trichoderma virens-mediated resistance in tomato against Fusarium wilt involve the jasmonic and salicylic acid pathways. Mol Plant Pathol 19(4):870–882PubMedPubMedCentralCrossRefGoogle Scholar
  46. Joshi R (2018) A review of Fusarium oxysporum on its plant interaction and industrial use. J Med Plants Stud 6(3):112–115CrossRefGoogle Scholar
  47. Kavitha T, Nelson R (2013) Exploiting the biocontrol activity of Trichoderma spp against root rot causing phytopathogens. ARPN J Agric Biol Sci 8(7):571–574Google Scholar
  48. Khan M, Ashraf S, Rasool F, Salati K (2014) Field performance of Trichoderma species against wilt disease complex of chickpea caused by Fusarium oxysporum f. sp. ciceri and Rhizoctonia solani. Turkish J Agric For 38(4):447–454CrossRefGoogle Scholar
  49. Khan B, Akash Z, Asad S et al (2017) Antagonistic potential of Trichoderma harzianum against Fusarium oxysporum f. sp. Cubense associated with panama wilt of banana. Pak J Phytopathol 29(1):111–116CrossRefGoogle Scholar
  50. 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
  51. Kumar DP, Thenmozhi R, Anupama A et al (2011) Selection of potential antagonistic Bacillus and Trichoderma isolates from tomato rhizosphere soil against Fusarium oxysporum f. sp. lycoperscisi. Res J Biol Sci 6(10):523–331CrossRefGoogle Scholar
  52. Lace B, Genre A, Woo S, Faccio A, Lorito M, Bonfante P (2014) Gate crashing arbuscular mycorrhizas: in vivo imaging shows the extensive colonization of both symbionts by Trichoderma atroviride. Environ Microbiol Rep 7(1):64–77PubMedCrossRefGoogle Scholar
  53. Li N, Alfiky A, Wang W, Islam M et al (2018) Volatile compound-mediated recognition and inhibition between Trichoderma biocontrol agents and Fusarium oxysporum. Front Microbiol 9:2614.  https://doi.org/10.3389/fmicb.2018.02614CrossRefPubMedPubMedCentralGoogle Scholar
  54. Lopez-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
  55. Maischak H, Zimmermann MR, Felle HH, Boland W, Mithofer A (2010) Alamethicin-induced electrical long distance signaling in plants. Plant Signal Behav 5:988–990PubMedPubMedCentralCrossRefGoogle Scholar
  56. Martınez-Medina A, Pascual JA, Lloret E, Roldan A (2009) Interactions between arbuscular mycorrhizal fungi and Trichoderma harzianum and their effects on Fusarium wilt in melon plants grown in seedling nurseries. J Sci Food Agric 89:1843–1850CrossRefGoogle Scholar
  57. Meena M, Swapnil P, Zehra A, Dubey MK, Upadhyay RS (2017) Antagonistic assessment of Trichoderma spp. by producing volatile and nonvolatile compounds against different fungal pathogens. Arch Phytopathol Plant Protect 50:629–648CrossRefGoogle Scholar
  58. Mei LI, Guang-shu MA, Hua L, Xiao-lin SU, Ying T, Wen-kun H, Jie M, Xiliang J (2019) The effects of Trichoderma on preventing cucumber Fusarium wilt and regulating cucumber physiology. J Integr Agric 18(3):607–617CrossRefGoogle Scholar
  59. Mendgen K, Hahn M, Deising H (1996) Morphogenesis and mechanisms of penetration by plant pathogenic fungi. Annu Rev Phytopathol 34(1):367–386PubMedCrossRefGoogle Scholar
  60. Miller SA, Rowe RC, Riedel RM (2011) Fusarium and Verticillium wilts of tomato, potato, pepper, and eggplant. Fact Sheet. Ohio State University, ColumbusGoogle Scholar
  61. Ming Q, Su C, Zheng C, Jia M, Zhang Q, Zhang H, Rahman K, Han T, Qin L (2013) Elicitors from the endophytic fungus Trichoderma atroviride promote Salvia miltiorrhiza hairy root growth and tanshinone biosynthesis. J Exp Bot 64(18):5687–5694PubMedPubMedCentralCrossRefGoogle Scholar
  62. Moraga-Suazo P, Opazo A, Zaldua S, Gonzalez G, Sanfuentes E (2011) Evaluation of Trichoderma spp. and Clonostachys spp. strains to control Fusarium circinatum in Pinus radiata seedlings. Chil J Agric Res 71:412–417CrossRefGoogle Scholar
  63. Moran-Diez E, Rubio B, Dominguez S, Hermosa R, Monte E, Nicolas C (2012) Transcriptomic response of Arabidopsis thaliana after 24h incubation with the biocontrol fungus Trichoderma harzianum. J Plant Physiol 169:614–620PubMedCrossRefGoogle Scholar
  64. Mueller WC, Beckman CH (1988) Correlated light and electron microscope studies of callose deposits in vascular parenchyma cells of tomato plants inoculated with Fusarium oxysporum f. sp. lycopersici. Physiol Mol Plant Pathol 33:201–208CrossRefGoogle Scholar
  65. Mukherjee PK, Kenerley CM (2010) Regulation of morphogenesis and biocontrol properties in Trichoderma virens by a VELVET protein, Vel1. Appl Environ Microbiol 76:2345–2352PubMedPubMedCentralCrossRefGoogle 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 PK, Wiest A, Ruiz N et al (2011) Two classes of new peptaibols are synthesized by a single non-ribosomal peptide synthetase of Trichoderma virens. J Biol Chem 286:4544–4554PubMedCrossRefGoogle Scholar
  68. Mukherjee M, Mukherjee PK, Horwitz BA et al (2012a) Trichoderma–plant–pathogen interactions: advances in genetics of biological control. Indian J Microbiol 52(4):522–529PubMedPubMedCentralCrossRefGoogle Scholar
  69. Mukherjee PK, Horwitz BA, Kenerley CM (2012b) Secondary metabolism in Trichoderma – a genomic perspective. Microbiology 158:35–45PubMedPubMedCentralCrossRefGoogle Scholar
  70. Naik MK, Madhukar HM, Rani GSD (2009) Evaluation of biocontrol efficacy of Trichoderma isolates and methods of its application against wilt of chilli (Capsicum annuum L.) caused by Fusarium solani (Mart) Sacc. J Biol Cont 23(1):31–36CrossRefGoogle Scholar
  71. Neer EJ (1995) Heterotrimeric G proteins: organizers of transmembrane signals. Cell 80(2):249–257PubMedCrossRefGoogle Scholar
  72. Nosir WS (2016) Trichoderma harzianum as a growth promoter and bio-control agent against Fusarium oxysporum f. sp. tuberosi. Adv Crop Sci Tech 4:217.  https://doi.org/10.4172/2329-8863.1000217CrossRefGoogle Scholar
  73. Nwankiti A, Gwa V (2018) Evaluation of antagonistic effect of Trichoderma harzianum against Fusarium oxysporum causal agent of white yam (Dioscorea rotundata poir) tuber rot. Trends Tech Sci Res 1(1):555554Google Scholar
  74. Okungbowa FI, Shittu HO (2012) Fusarium wilts: an overview. Environ Res J 6(2):83–102Google Scholar
  75. Omann MR, Lehner S, Rodriguez CE, Brunner K, Zeilinger S (2012) The seven-transmembrane receptor Gpr1 governs processes relevant for the antagonistic interaction of Trichoderma atroviride with its host. Microbiology 158:107–118PubMedPubMedCentralCrossRefGoogle Scholar
  76. Ortiz E, Cruz M, Melgarejo LM, Marquinez X, Hoyos-Carvajal L (2014) Histopathological features of infections caused by Fusarium oxysporum and F. solani in purple passion fruit plants (Passiflora edulis Sims). Summa Phytopathol 40(2):134–140CrossRefGoogle Scholar
  77. Pandey V, Shukla A, Kumar J (2016) Physiological and molecular signalling involved in disease management through Trichoderma: an effective biocontrol paradigm. In: Kumar P, Gupta V, Tiwari A, Kamle M (eds) Current trends in plant disease diagnostics and management practices. Fungal biology. Springer, Cham, pp 317–346CrossRefGoogle Scholar
  78. Patole SP, Dhore SB, Pradhan RS, Shankara K (2017) In vitro evaluation of Trichoderma viride and Trichoderma harzianum against Fusarium wilt of chickpea. Int J Pure App Biosci 5(5):460–464CrossRefGoogle Scholar
  79. Petrisor C, Paica A, Constantinescu F (2017) Effect of secondary metabolites produced by different Trichoderma spp. isolates against Fusarium oxysporum f. sp. radicis-lycopersici and Fusarium solani. Sci Pap B Hortic 61:407–411Google Scholar
  80. Pitt JI, Hocking AD, Bhudhasamai K et al (1994) The normal mycoflora of commodities from Thailand. 2. Beans, rice, small grains and other commodities. Int J Food Microbiol 23:35–43PubMedCrossRefGoogle Scholar
  81. Qualhato FT, Cardoso-Lopes FA, Steindorff AS et al (2013) Mycoparasitism studies of Trichoderma species against three phytopathogenic fungi: evaluation of antagonism and hydrolytic enzyme production. Biotechnol Lett 35:1461–1468PubMedCrossRefGoogle Scholar
  82. Raaijmakers JM, Paulitz TC, Steinberg C et al (2009) The rhizosphere: a playground and battlefield for soil borne pathogens and beneficial microorganisms. Plant Soil 321:341–361CrossRefGoogle Scholar
  83. Rajeswari P (2019) Combination of Trichoderma viride and Pseudomonas fluorescens for the enhanced control of Fusarium wilt disease caused by Fusarium oxysporum infecting Arachis hypogaea L. J Appl Nat Sci 11(1):138–143CrossRefGoogle Scholar
  84. Redda ET, Ma J, Mei J, Li M, Wu B, Jiang X (2018) Antagonistic potential of different isolates of Trichoderma against Fusarium oxysporum, Rhizoctonia solani, and Botrytis cinerea. Eur J Exp Biol 8:1–8Google Scholar
  85. Reino JL, Guerrero RF, Hernandez-Galan R, Collado IG (2008) Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochem Rev 7:89–123CrossRefGoogle Scholar
  86. 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 42:749–760PubMedPubMedCentralCrossRefGoogle Scholar
  87. Rejeb IB, Pastor V, Mauch-Mani B (2014) Plant responses to simultaneous biotic and abiotic stress: molecular mechanisms. Plan Theory 3(4):458–475Google Scholar
  88. Rini CR, Sulochana KK (2007) Usefulness of Trichoderma and Pseudomonas against Rhizoctonia solani and Fusarium oxysporum infecting tomato. J Trop Agric 45:21–28Google Scholar
  89. Rippa S, Eid M, Formaggio F, Toniolo C, Beven L (2010) Hypersensitive-like response to the pore-former peptaibol alamethicin in Arabidopsis thaliana. ChemBioChem 11:2042–2049PubMedCrossRefGoogle Scholar
  90. 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
  91. Saravanakumar K, Li Y, Yu C, Wang Q, Wang M, Sun J, Gao J, Chen J (2017) Effect of Trichoderma harzianum on maize rhizosphere microbiome and biocontrol of Fusarium stalk rot. Sci Rep 7:1771.  https://doi.org/10.1038/s41598-017-01680-wCrossRefPubMedPubMedCentralGoogle Scholar
  92. Sarma BK, Yadav SK, Patel JS, Singh HB (2014) Molecular mechanisms of interactions of Trichoderma with other fungal species. Open Mycol J 8:140–147CrossRefGoogle Scholar
  93. Schmoll M (2008) The information highways of a biotechnological workhorse-signal transduction in Hypocrea jecorina. BMC Genomics 9:430PubMedPubMedCentralCrossRefGoogle Scholar
  94. Shi M, Chen L, Wang XW, Zhan T et al (2012) Antimicrobial peptaibols from Trichoderma pseudokoningii induce programmed cell death in plant fungal pathogens. Microbiology 158:166–175PubMedCrossRefGoogle Scholar
  95. Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43PubMedPubMedCentralCrossRefGoogle Scholar
  96. Silva VN, Fernandes FMC, Cortez A et al (2006) Characterization and genetic variability of Fusarium verticillioides strains isolated from corn and sorghum in Brazil based on fumonisins production, microsatellites, mating type locus, and mating crosses. Can J Microbiol 52:798–804PubMedCrossRefGoogle Scholar
  97. Sinha A, Harshita Singh R, Verma A (2018) Bioefficacy of Trichoderma harzianum and Trichoderma viride against Fusarium oxysporum f. sp. capsici causing wilt disease in chilli. J Pharmacog Phytochem 7(5):965–966Google Scholar
  98. Stankovic S, Levic J, Petrovic T, Logrieco A, Moretti A (2007) Pathogenicity and mycotoxin production by Fusarium proliferatum isolated from onion and garlic in Serbia. Eur J Plant Pathol 118:165–172CrossRefGoogle Scholar
  99. Taribuka J, Wibowo A, Widyastuti SM, Sumardiyono C (2017) Potency of six isolates of biocontrol agents endophytic Trichoderma against Fusarium wilt on banana. J Degrade Min Land Manage 4:723–731CrossRefGoogle Scholar
  100. 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
  101. Vargas WA, Crutcher FK, Kenerley CM (2011) Functional characterization of a plant-like sucrose transporter from the beneficial fungus Trichoderma virens. Regulation of the symbiotic association with plants by sucrose metabolism inside the fungal cells. New Phytol 189:777–789PubMedCrossRefGoogle Scholar
  102. Verma NP, Kaur I, Masih H, Singh AK, Singla A (2017) Efficacy of Trichoderma in controlling Fusarium wilt in tomato (Solanum lycopersicum L.). Res Environ Life Sci 10(7):636–639Google Scholar
  103. Verma NP, Kuldeep YK, Sinha BK (2018) Efficacy of indigenous Trichoderma strain bio-control against of Fusarium sp. tomato plant causal agent of (Solanum lycopersicon L.) in vitro condition. Int J Curr Microbiol App Sci 7(3):1578–1584CrossRefGoogle Scholar
  104. Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Woo SL, Lorito M (2008) Trichoderma-plant-pathogen interactions. Soil Biol Biochem 40:1–10CrossRefGoogle Scholar
  105. Vinale F, Ghisalberti EL, Sivasithamparam K et al (2009) Factors affecting the production of Trichoderma harzianum secondary metabolites during the interaction with different plant pathogens. Lett Appl Microbiol 48:705–711PubMedPubMedCentralGoogle Scholar
  106. Viterbo A, Horwotz BA (2010) Mycoparasitism. In: Borkovich KA, Ebbole DJ (eds) Cellular and molecular biology of filamentous fungi. ASM Press, Herndon, pp 676–694Google Scholar
  107. Viterbo A, Wiest A, Brotman Y, Chet I, Kenerley C (2007) The 18mer peptaibols from Trichoderma virens elicit plant defence responses. Mol Plant Pathol 8:737–746PubMedPubMedCentralCrossRefGoogle Scholar
  108. Wang M, Dong Y, Zhao Q, Wang F, Liu K, Jiang B, Fang X (2014) Identification of the role of a MAP kinase Tmk2 in Hypocreajecorina (Trichoderma reesei). Sci Rep 4:6732.  https://doi.org/10.1038/srep06732CrossRefPubMedPubMedCentralGoogle Scholar
  109. Wani AH, Taskeen-Un-Nisa, Mir RA (2009) Biological control of Fusarium oxysporum f. sp. lycopercici on tomato with fungal antagonists. J Biol Cont 23(2):169–173Google Scholar
  110. Yedidia I, Srivastva AK, Kapulnik Y, Chet I (2001) Effect of Trichoderma harzianum on microelement concentrations and increased growth of cucumber plants. Plant Soil 235:235–242CrossRefGoogle Scholar
  111. Zeilinger S, Gruber S, Bansal R, Mukherjee PK (2016) Secondary metabolism in Trichoderma-chemistry meets genomics. Fungal Biol Rev 30:74–90CrossRefGoogle Scholar
  112. Zhang F, Zhu Z, Yang XM, Ran W, Shen Q (2013a) Trichoderma harzianum T-E5 significantly affects cucumber root exudates and fungal community in the cucumber rhizosphere. Appl Soil Ecol 72:41–48CrossRefGoogle Scholar
  113. Zhang F, Yuan J, Yang X, Cui Y, Chen L, Ran W, Shen Q (2013b) Putative Trichoderma harzianum mutant promotes cucumber growth by enhanced production of indole acetic acid and plant colonization. Plant Soil 368:433–444CrossRefGoogle Scholar
  114. Zhang F, Yang X, Ran W, Shen Q (2014) Fusarium oxysporum induces the production of proteins and volatile organic compounds by Trichoderma harzianum TE-5. FEMS Microbiol Lett 359:116–123PubMedPubMedCentralCrossRefGoogle Scholar
  115. Zhang F, Huo Y, Cobb AB, Luo G, Zhou J, Yang G, Wilson GWT, Zhang Y (2018) Trichoderma biofertilizer links to altered soil chemistry, altered microbial communities, and improved grassland biomass. Front Microbiol 9:848.  https://doi.org/10.3389/fmicb.2018.00848CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2020

Authors and Affiliations

  • Ishwar Prakash Sharma
    • 1
  • Anil K. Sharma
    • 1
  1. 1.Biological Sciences, CBSHG.B. Pant University of Agriculture & TechnologyPantnagarIndia

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