Abstract
An increasing human population will lead to a higher demand for food, posing significant global challenges. To achieve sustainable agriculture, utilizing microorganisms is a promising alternative to chemical fertilizers and pesticides, minimizing risks to both the environment and the food chain. The utilization of Trichoderma fungus is considered one of the most effective eco friendly practices and has garnered significant attention due to its opportunistic nature and co mopolitan distribution. Notably, Trichoderma spp. in agroecosystems not only exhibit efficacy against phytopathogens and pests as biocontrol agents but also serve as valuable and convenient models in agricultural studies and environmental evaluations. Although these fungi are renowned for their numerous beneficial effects, they carry a potential risk of contamination to different species of mushrooms. In conclusion, this review sheds light on the multifaceted role of Trichoderma in both plant health and environmental contexts. This study provides a comprehensive overview of its mechanism of action and pathways, metabolite production, and checklists for biocontrol, formulation, and bioremediation. The current limited understanding of the effects of Trichoderma spp. in agroecosystems emphasizes the necessity for comprehensive studies to uncover its functions and roles. Conducting extensive research on the interactions of Trichoderma within diverse agricultural ecosystems will clarify its contributions to various aspects, including plant growth and well-being, nutrient cycling, soil fertility, disease suppression, microbial communities, overall sustainability, and potentially other ecosystem services.
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References
Abbas A, Mubeen M, Zheng H, Sohail MA et al (2022) Trichoderma spp. genes Involved in the biocontrol activity against Rhizoctonia solani. Front Microbiol 13:884469. https://doi.org/10.3389/fmicb.2022.88446
Abdel-Lateff A, Fisch K, Wright AD (2009) Trichopyrone and other constituents from the marine sponge-derived fungus Trichoderma sp. Z Naturforsch C 64:186–192. https://doi.org/10.1515/znc-2009-3-406
Abe N, Yamamoto K, Hirota A (2000) Novel fungal metabolites, demethylsorbicillin and oxosorbicillinol, isolated from Trichoderma sp. USF-2690. Biosci Biotechnol Biochem 64:620–622. https://doi.org/10.1271/bbb.64.620
Affokpon A, Coyne DL, Htay CC, Agbèdè RD et al (2011) Biocontrol potential of native Trichoderma isolates against root-knot nematodes in West African vegetable production systems. Soil Biol Biochem 43:600–608. https://doi.org/10.1016/j.soilbio.2010.11.029
Agency U S E P (2021) Biopesticide active ingredients. https://www.epa.gov/ingredients-used-pesticide-products/biopesticide-active-ingredients
Ahluwalia V, Walia S, Sati OP, Kumar J et al (2014) Isolation, characterisation of major secondary metabolites of the Himalayan Trichoderma koningii and their antifungal activity. Arch Phytopathol Plant Prot 47:1063–1071. https://doi.org/10.1080/03235408.2013.829715
AL-Shammari TA, Bahkali AH, Elgorban AM, El-Kahky MT, Al-Sum BA (2013) The use of Trichoderma longibrachiatum and Mortierella alpina against root-knot nematode, Meloidogyne javanica on tomato. J Pure Appl Microbiol 7:199–207
Alizadeh M, Vasebi Y, Safaie N (2020) Microbial antagonists against plant pathogens in Iran: a review. Open Agric 5(1):404–440. https://doi.org/10.1515/opag-2020-0031
Alizadeh M, Vasebi Y, Chauhan M, Rani A (2021) Biopriming: a prospective techniques for crop improvement. Innovations 66:1035–1058
Alonso-Ramírez A, Poveda J, Martín I, Hermosa R et al (2014) Salicylic acid prevents Trichoderma harzianum from entering the vascular system of roots. Mol Plant Pathol 15:823–831. https://doi.org/10.1111/mpp.12141
de Andrade LA, Santos CHB, Frezarin ET, Sales LR, Rigobelo EC (2023) Plant growth-promoting rhizobacteria for sustainable agricultural production. Microorganisms 11:1088. https://doi.org/10.3390/microorganisms11041088
Andrade R, Ayer WA, Mebe PP (1992) The metabolites of Trichoderma longibrachiatum. Part 1. Isolation of the metabolites and the structure of trichodimerol. Can J Chem 70:2526–2535. https://doi.org/10.1139/v92-320
Andrade R, Ayer WA, Trifonov LS (1997) The metabolites of Trichoderma longibrachiatum. III. two new tetronic acids: 5 hydroxyvertinolideand bislongiquinolide. Aust J Chem 50:255–258. https://doi.org/10.1071/C96103
Aro N, Ilmén M, Saloheimo A, Penttilä M (2003) ACEI of Trichoderma reesei is a repressor of cellulase and xylanase expression. Appl Environ Microbiol 69:56–65. https://doi.org/10.1128/AEM.69.1.56-65.2003
Arora NK, Khare E, Maheshwari DK (2011) Plant growth promoting Rhizobacteria: constraints in bioformulation, commercialization, and future strategies. In: Plant growth and health promoting bacteria. Springer, Berlin, Heidelberg, pp 97–116 https://doi.org/10.1007/978-3-642-13612-2_5
Asad SA, Ali N, Hameed A, Khan SA et al (2014) Biocontrol efficacy of different isolates of Trichoderma against soil borne pathogen Rhizoctonia solani. Pol J Microbiol 63:95–103
Avni A, Bailey BA, Mattoo AK, Anderson JD (1994) Induction of ethylene biosynthesis in Nicotiana tabacum by a Trichoderma viride xylanase is correlated to the accumulation of 1‑Aminocyclopropane-1-Carboxylic Acid (ACC) synthase and ACC oxidase transcripts. Plant Physiol 106:1049–1055. https://doi.org/10.1104/pp.106.3.1049
Backman P, Rodriguez-Kabana R (1975) A system for the growth and delivery of biological control agents to the soil. Phytopathology 65:3–21. https://doi.org/10.1094/Phyto-65-819
Baek J‑M, Howell CR, Kenerley CM (1999) The role of an extracellular chitinase from Trichoderma virens Gv29‑8 in the biocontrol of Rhizoctonia solani. Curr Genet 35:41–50. https://doi.org/10.1007/s002940050431
Bailey BA, Dean JFD, Anderson JD (1990) An ethylene biosynthesis-inducing endoxylanase elicits electrolyte leakage and necrosis in Nicotiana tabacum cv Xanthi leaves 1. Plant Physiol 94:1849–1854. https://doi.org/10.1104/pp.94.4.1849
Baldoni DB, Antoniolli ZI, Mazutti MA, Jacques RJS et al (2020) Chitinase production by Trichoderma koningiopsis UFSMQ40 using solid state fermentation. Braz J Microbiol 51:1897–1908. https://doi.org/10.1007/s42770-020-00334-w
Bankole SA, Adebanjo A (1996) Biocontrol of brown blotch of cowpea caused by Colletotrichum truncatum with Trichoderma viride. Crop Prot 15:633–636. https://doi.org/10.1016/0261-2194(96)00028-2
Batta YA (2007) Control of postharvest diseases of fruit with an invert emulsion formulation of Trichoderma harzianum Rifai. Postharvest Biol Technol 43:143–150. https://doi.org/10.1016/j.postharvbio.2006.07.010
Begum MF, Rahman M, Alam MF (2010) Biological control of Alternaria fruit rot of chili by Trichoderma species under field conditions. Mycobiology 38:113–117. https://doi.org/10.4489/MYCO.2010.38.2.113
Bellemain E, Carlsen T, Brochmann C, Coissac E et al (2010) ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases. BMC Microbiol 10:189. https://doi.org/10.1186/1471-2180-10-189
Benítez T, Rincón AM, Limón MC, Codon AC (2004) Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7:249–260
Benttoumi N, Colagiero M, Sellami S, Boureghda H et al (2020) Diversity of nematode microbial antagonists from Algeria shows occurrence of nematotoxic Trichoderma spp. Plants 9:941. https://doi.org/10.3390/plants9080941
Berg A, Kemami Wangun HV, Nkengfack AE, Schlegel B (2004) Lignoren, a new sesquiterpenoid metabolite from Trichoderma lignorum HKI 0257. J Basic Microbiol 44:317–319. https://doi.org/10.1002/jobm.200410383
Bills GF, Gloer JB (2017) Biologically active secondary metabolites from the fungi. Microbiol Spectr. https://doi.org/10.1128/microbiolspec.FUNK-0009-2016
Bokhari FM (2009) Efficacy of some Trichoderma species in the control of Rotylenchulus reniformis and Meloidogyne javanica. Arch Phytopathol Plant Prot 42:361–369. https://doi.org/10.1080/03235400601070520
Bolton MD, Thomma BPHJ, Nelson BD (2006) Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Mol Plant Pathol 7:1–16. https://doi.org/10.1111/j.1364-3703.2005.00316.x
Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48. https://doi.org/10.1038/ncomms1046
Braithwaite M, Clouston A, Minchin R, Yardley J et al (2016) The density-dependent effect of initial nematode population levels on the efficacy of Trichoderma as a bio-nematicide against Meloidogyne hapla on tomato. Aust Plant Pathol 45:473–479. https://doi.org/10.1007/s13313-016-0432-5
Brakhage AA (2013) Regulation of fungal secondary metabolism. Nat Rev Microbiol 11:21–32. https://doi.org/10.1038/nrmicro2916
Brakhage AA, Schroeckh V (2011) Fungal secondary metabolites – Strategies to activate silent gene clusters. Fungal Genet Biol 48:15–22. https://doi.org/10.1016/j.fgb.2010.04.004
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. https://doi.org/10.1104/pp.108.116293
Brotman Y, Lisec J, Meret M, Chet I et al (2012) Transcript and metabolite analysis of the Trichoderma-induced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana. Microbiology 158:139–146. https://doi.org/10.1099/mic.0.052621-0
Cai F, Yu G, Wang P, Wei Z et al (2013) Harzianolide, a novel plant growth regulator and systemic resistance elicitor from Trichoderma harzianum. Plant Physiol Biochem 73:106–113. https://doi.org/10.1016/j.plaphy.2013.08.011
Calderón AA, Zapata JM, Muñoz R, Pedreño MA, Barceló 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. https://doi.org/10.1111/j.1469-8137.1993.tb03836.x
Cardoza R‑E, Hermosa M‑R, Vizcaíno J‑A, Sanz L et al (2005) Secondary metabolites produced by Trichoderma and their importance in the biocontrol process. In: Microorganism for industrial enzymes and biocontrol, pp 1–22 https://doi.org/10.1016/j.fbr.2016.05.001
Carrero-Carrón I, Trapero-Casas JL, Olivares-García C, Monte E et al (2016) Trichoderma asperellum is effective for biocontrol of Verticillium wilt in olive caused by the defoliating pathotype of Verticillium dahliae. Crop Prot 88:45–52. https://doi.org/10.1016/j.cropro.2016.05.009
Chacón MR, Rodríguez-Galán O, Benítez T, Sousa S et al (2007) Microscopic and transcriptome analyses of early colonization of tomato roots by Trichoderma harzianum. Int Microbiol 10:19
Chen L, Niu S‑B, Li L, Ding G et al (2017) Trichoderpyrone, a unique polyketide hybrid with a cyclopentenone-pyrone skeleton from the plant endophytic fungus Trichoderma gamsii. J Nat Prod 80:1944–1947. https://doi.org/10.1021/acs.jnatprod.7b00190
Chen L‑H, Cui Y‑Q, Yang X‑M, Zhao D‑K, Shen Q‑R (2012) An antifungal compound from Trichoderma harzianum SQR-T037 effectively controls Fusarium wilt of cucumber in continuously cropped soil. Aust Plant Pathol 41:239–245. https://doi.org/10.1007/s13313-012-0119-5
Chet I, Spiegel Y, Sharon E (2004) Mechanisms and improved biocontrol of the root-knot nematodes by Trichoderma spp. InVI International Symposium on Chemical and non-Chemical Soil and Substrate Disinfestation-SD2004 698 (pp. 225–228). https://doi.org/10.17660/ActaHortic.2005.698.30
Contina J, Dandurand L, Knudsen G (2017) Use of GFP-tagged Trichoderma harzianum as a tool to study the biological control of the potato cyst nematode Globodera pallida. Appl Soil Ecol 115:31–37. https://doi.org/10.1016/j.apsoil.2017.03.010
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. https://doi.org/10.1104/pp.108.130369
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 fungi Botrytis cinerea. Plant Signal Behav 6:1554–1563. https://doi.org/10.4161/psb.6.10.17443
Contreras-Cornejo HA, Macías-Rodríguez L, Alfaro-Cuevas R, López-Bucio J (2014) Trichoderma spp. improve growth of Arabidopsis seedlings under salt stress through enhanced root development, osmolite production, and na+ elimination through root exudates. Mol Plant Microbe Interact 27:503–514. https://doi.org/10.1094/mpmi-09-13-0265-r
d Costa SDA, Cardoso AF, d Castro GLS, d Júnior DDS et al (2022) Co-Inoculation of Trichoderma asperellum with Bacillus subtilis to promote growth and nutrient absorption in Marandu Grass. Appl Environ Soil Sci 2022:3228594. https://doi.org/10.1155/2022/3228594
Crutcher FK, Parich A, Schuhmacher R, Mukherjee PK et al (2013) A putative terpene cyclase, vir4, is responsible for the biosynthesis of volatile terpene compounds in the biocontrol fungus Trichoderma virens. Fungal Genet Biol 56:67–77. https://doi.org/10.1016/j.fgb.2013.05.003
Crutcher FK, Moran-Diez ME, Ding S, Liu J et al (2015) A paralog of the proteinaceous elicitor SM1 is involved in colonization of maize roots by Trichoderma virens. Fungal Biol 119:476–486. https://doi.org/10.1016/j.funbio.2015.01.004
Cuevas VC, Sinohin AM (2005) Performance of selected Philippine species of Trichoderma as biocontrol agents of damping off pathogens and as growth enhancer of vegetables in farmers’ field. Philipp Agric Sci.
Cui J, Shang R‑Y, Sun M, Li Y‑X et al (2020) Trichodermaloids A–C, cadinane sesquiterpenes from a marine sponge symbiotic Trichoderma sp. SM16 fungus. Chem Biodivers 17:e2000036. https://doi.org/10.1002/cbdv.202000036
Cumagun CJR (2014) Advances in formulation of Trichoderma for biocontrol. In: Biotechnology and biology of Trichoderma. Elsevier, Amsterdam, pp 527–531 https://doi.org/10.1016/B978-0-444-59576-8.00039-4
Cutler HG, Himmelsbach DS, Arrendale RF, Cole PD, Cox RH (1989) Koninginin A: A novel plant growth regulator from Trichoderma koningii. Agric Biol Chem 53:2605–2611. https://doi.org/10.1080/00021369.1989.10869746
Cutler HG, Cutler SJ, Ross SA, Sayed KE et al (1999) Koninginin G, a new metabolite from Trichoderma aureoviride. J Nat Prod 62:137–139. https://doi.org/10.1021/np9801817
Daragó Á, Szabó M, Hrács K, Takács A, Nagy P (2013) In vitro investigations on the biological control of Xiphinema index with Trichoderma species. Helminthologia 50:132–137
Das B, Das B, Dutta P, Sarmah D (2006) Bioformulation of Trichoderma harzianum Rifai for management of soybean stem-rot caused by Rhizoctonia solani Kuhn. J Biol Control: 57–64
Datnoff L, Nemec S, Pernezny K (1995) Biological control of Fusarium crown and root rot of tomato in Florida using Trichoderma harzianum and Glomus intraradices. Biol Control 5:427–431. https://doi.org/10.1006/bcon.1995.1051
Dean J, Gamble H, Anderson J (1989) The ethylene biosynthesis-inducing xylanase: its induction in Trichoderma viride and certain plant pathogens. Phytopathology 79:1071–1078
Díaz-Gutiérrez C, Arroyave C, Llugany M, Poschenrieder C et al (2021) Trichoderma asperellum as a preventive and curative agent to control Fusarium wilt in Stevia rebaudiana. Biol Control 155:104537. https://doi.org/10.1016/j.biocontrol.2021.104537
Ding G, Chen AJ, Lan J, Zhang H et al (2012a) Sesquiterpenes and cyclopeptides from the endophytic fungus Trichoderma asperellum Samuels, Lieckf. & Nirenberg. Chem Biodivers 9:1205–1212. https://doi.org/10.1002/cbdv.201100185
Ding G, Wang H, Li L, Chen AJ et al (2012b) Trichoderones A and B: Two pentacyclic cytochalasans from the plant endophytic fungus Trichoderma gamsii. Eur J Org Chem 2012:2516–2519. https://doi.org/10.1002/ejoc.201200053
Ding G, Chen L, Chen A, Tian X et al (2012c) Trichalasins C and D from the plant endophytic fungus Trichoderma gamsii. Fitoterapia 83:541–544. https://doi.org/10.1016/j.fitote.2011.12.021
Ding G, Chen L, Zhou C, Hong-Mei J et al (2015) Trichoderamides A and B, a pair of stereoisomers from the plant endophytic fungus Trichoderma gamsii. J Antibiot 68:409–413. https://doi.org/10.1038/ja.2015.1
Ding Z, Wang X, Kong F‑D, Huang H‑M et al (2020) Overexpression of global regulator talae1 leads to the discovery of new antifungal polyketides from endophytic fungus Trichoderma afroharzianum. Front Microbiol. https://doi.org/10.3389/fmicb.2020.622785
Djonović S, Vargas WA, Kolomiets MV, Horndeski M et al (2007) A proteinaceous elicitor sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol 145:875–889. https://doi.org/10.1104/pp.107.103689
Doni F, Isahak A, Che Mohd Zain CR, Mohd Ariffin S et al (2014) Formulation of Trichoderma sp. SL2 inoculants using different carriers for soil treatment in rice seedling growth. SpringerPlus 3:532. https://doi.org/10.1186/2193-1801-3-532
Driks A (2004) The bacillus spore coat. Phytopathology® 94:1249–1251. https://doi.org/10.1094/phyto.2004.94.11.1249
Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA et al (2011) Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9:749–759. https://doi.org/10.1038/nrmicro2637
Du F‑Y, Ju G‑L, Xiao L, Zhou Y‑M, Wu X (2020) Sesquiterpenes and cyclodepsipeptides from marine-derived fungus Trichoderma longibrachiatum and their antagonistic activities against soil-borne pathogens. Mar Drugs 18:165
Eddleston M, Nagami H, Lin C‑Y, Davis ML, Chang S‑S (2022) Pesticide use, agricultural outputs, and pesticide poisoning deaths in Japan. Clin Toxicol 60:933–941. https://doi.org/10.1080/15563650.2022.2064868
El-Katatny MH, Emam AS (2012) Control of postharvest tomato rot by spore suspension and antifungal metabolites of Trichoderma harzianum. J Microbiol Biotechnol Food Sci 1:1505–1528
Elad Y (2003) Biocontrol of foliar pathogens: mechanisms and application. Commun Agric Appl Biol Sci 68:17–24
Elad Y, Freeman S (2002) Biological control of fungal plant pathogens. In: Agricultural applications, pp 93–109
Elzawahry AM, Khalil A, Allam A, Mostafa RG (2015) Effect of the bio-agents (Bacillus megaterium and Trichoderma album) on citrus nematode (Tylenchulus semipenetrans) infecting baladi orange and. J Phytopathol Dis Manag: 1–8
Emmert EAB, Handelsman J (1999) Biocontrol of plant disease: a (Gram-) positive perspective. FEMS Microbiol Lett 171:1–9. https://doi.org/10.1111/j.1574-6968.1999.tb13405.x
Endo A, Hasumi K, Yamada A, Shimoda R, Takeshima H (1986) The synthesis of compactin (ML-236B) and monacolin K in fungi. J Antibiot 39:1609–1610. https://doi.org/10.7164/antibiotics.39.1609
Evidente A, Cabras A, Maddau L, Serra S et al (2003) Viridepyronone, a new antifungal 6‑Substituted 2H-Pyran-2-one produced by Trichoderma viride. J Agric Food Chem 51:6957–6960. https://doi.org/10.1021/jf034708j
Fan H, Yao M, Wang H, Zhao D et al (2020) Isolation and effect of Trichoderma citrinoviride Snef1910 for the biological control of root-knot nematode, Meloidogyne incognita. BMC Microbiol 20:1–11. https://doi.org/10.1186/s12866-020-01984-4
Fang F, Zhao J, Ding L, Huang C et al (2017) 5‑Hydroxycyclopenicillone, a new β‑Amyloid fibrillization inhibitor from a sponge-derived fungus Trichoderma sp. HPQJ-34. Mar Drugs 15:260. https://doi.org/10.3390/md15080260
Felix CR, Noronha EF, Miller RNG (2014) Trichoderma: a dual function fungi and their use in the wine and beer industries. In: Biotechnology and Biology of Trichoderma. Elsevier, Amsterdam, pp 345–349 https://doi.org/10.1016/B978-0-444-59576-8.00025-4
Ferreira FV, Herrmann-Andrade AM, Calabrese CD, Bello F et al (2020) Effectiveness of Trichoderma strains isolated from the rhizosphere of citrus tree to control Alternaria alternata, Colletotrichum gloeosporioides and Penicillium digitatum A21 resistant to pyrimethanil in post-harvest oranges (Citrus sinensis L.(Osbeck)). J Appl Microbiol 129:712–727. https://doi.org/10.1111/jam.14657
Fontenelle A, Guzzo S, Lucon C, 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. https://doi.org/10.1016/j.cropro.2011.07.019
de França SKS, Cardoso AF, Lustosa DC, Ramos EMLS et al (2015) Biocontrol of sheath blight by Trichoderma asperellum in tropical lowland rice. Agron Sustain Dev 35:317–324. https://doi.org/10.1007/s13593-014-0244-3
Freeman S, Minz D, Kolesnik I, Barbul O et al (2004) Trichoderma biocontrol of Colletotrichum acutatum and Botrytis cinerea and survival in strawberry. Eur J Plant Pathol 110:361–370. https://doi.org/10.1023/B:EJPP.0000021057.93305.d9
Frischmann A, Neudl S, Gaderer R, Bonazza K et al (2013) Self-assembly at air/water interfaces and carbohydrate binding properties of the small secreted protein EPL1 from the fungus Trichoderma atroviride. J Biol Chem 288:4278–4287. https://doi.org/10.1074/jbc.M112.427633
Gaderer R, Lamdan NL, Frischmann A, Sulyok M et al (2015) Sm2, a paralog of the Trichoderma cerato-platanin elicitor Sm1, is also highly important for plant protection conferred by the fungal-root interaction of Trichoderma with maize. BMC Microbiol 15:2. https://doi.org/10.1186/s12866-014-0333-0
Gallo A, Mulè G, Favilla M, Altomare C (2004) Isolation and characterisation of a trichodiene synthase homologous gene in Trichoderma harzianum. Physiol Mol Plant Pathol 65:11–20. https://doi.org/10.1016/j.pmpp.2004.11.005
Gardener BBM, Fravel DR (2002) Biological control of plant pathogens: research, commercialization, and application in the USA. Plant Health Prog 3:17. https://doi.org/10.1094/php-2002-0510-01-rv
Garnica-Vergara A, Barrera-Ortiz S, Muñoz-Parra E, Raya-González J et al (2016) The volatile 6‑pentyl-2H-pyran-2-one from Trichoderma atroviride regulates Arabidopsis thaliana root morphogenesis via auxin signaling and ethylene insensitive 2 functioning. New Phytol 209:1496–1512. https://doi.org/10.1111/nph.13725
Ghisalberti EL, Sivasithamparam K (1991) Antifungal metabolites from Trichoderma harzianum. J Nat Prod 56:1799–1804. https://doi.org/10.1021/np50100a020
Gong B, Zhang S, Lin Y, Wang X et al (2013) Study on metabolites with antifungal activity against plant pathogens of an endophytic fungus Trichoderma sp. 09 from Myoporum bontioides A. Gray. Guangdong Agric Sci 40:62–65
Guzmán-Guzmán P, Alemán-Duarte MI, Delaye L, Herrera-Estrella A, Olmedo-Monfil V (2017) Identification of effector-like proteins in Trichoderma spp. and role of a hydrophobin in the plant-fungus interaction and mycoparasitism. BMC Genet 18:16. https://doi.org/10.1186/s12863-017-0481-y
Guzmán-Guzmán P, Porras-Troncoso MD, Olmedo-Monfil V, Herrera-Estrella A (2019) Trichoderma species: versatile plant symbionts. Phytopathology® 109:6–16. https://doi.org/10.1094/phyto-07-18-0218-rvw
Hanada RE, Pomella AW, Soberanis W, Loguercio LL, Pereira JO (2009) Biocontrol potential of Trichoderma martiale against the black-pod disease (Phytophthora palmivora) of cacao. Biol Control 50:143–149. https://doi.org/10.1016/j.biocontrol.2009.04.005
Hanson LE, Howell CR (2004) Elicitors of plant defense responses from biocontrol strains of Trichoderma viren. Phytopathology® 94:171–176. https://doi.org/10.1094/phyto.2004.94.2.171
Haran S, Schickler H, Chet I (1996) Molecular mechanisms of lytic enzymes involved in the biocontrol activity of Trichoderma harzianum. Microbiology 142:2321–2331. https://doi.org/10.1099/00221287-142-9-2321
Harman GE, Lorito M, Lynch J (2004a) Uses of Trichoderma spp. to alleviate or remediate soil and water pollution. In: Advances in applied microbiology. Academic Press, pp 313–330 https://doi.org/10.1016/S0065-2164(04)56010-0
Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004b) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56. https://doi.org/10.1038/nrmicro797
Harman GE, Herrera-Estrella AH, Horwitz BA, Lorito M (2012) Trichoderma—from basic biology to biotechnology. Microbiology 158:1–2. https://doi.org/10.1099/mic.0.056424-0
Harwoko H, Daletos G, Stuhldreier F, Lee J et al (2021) Dithiodiketopiperazine derivatives from endophytic fungi Trichoderma harzianum and Epicoccum nigrum. Nat Prod Res 35:257–265. https://doi.org/10.1080/14786419.2019.1627348
Hirose A, Maeda H, Tonouchi A, Nehira T, Hashimoto M (2014) Neomacrophorin I, II, and III, novel drimenyl cyclohexanes with hydroxylated butanoates from Trichoderma sp. 1212–03. Tetrahedron 70:1458–1463. https://doi.org/10.1016/j.tet.2013.12.087
Howell CR (2002) Cotton seedling preemergence damping-off incited by Rhizopus oryzae and Pythium spp. and its biological control with Trichoderma spp. Phytopathology® 92:177–180. https://doi.org/10.1094/phyto.2002.92.2.177
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. https://doi.org/10.1094/pdis.2003.87.1.4
Howell CR, Stipanovic RD, Lumsden RD (1993) Antibiotic production by strains of Gliocladium virens and its relation to the biocontrol of cotton seedling diseases. Biocontrol Sci Technol 3:435–441. https://doi.org/10.1080/09583159309355298
Iida A, Sanekata M, Fujita T, Tanaka H et al (1994) Fungal metabolites. XVI. Structures of new peptaibols, trichokindins I–VII, from the fungus Trichoderma harzianum. Chem Pharm Bull 42:1070–1075. https://doi.org/10.1248/cpb.42.1070
Intana W, Kheawleng S, Sunpapao A (2021) Trichoderma asperellum T76-14 released volatile organic compounds against postharvest fruit rot in muskmelons (Cucumis melo) caused by Fusarium incarnatum. J Fungi 7:46. https://doi.org/10.3390/jof7010046
Jambhulkar PP, Sharma P, Manokaran R, Lakshman DK et al (2018) Assessing synergism of combined applications of Trichoderma harzianum and Pseudomonas fluorescens to control blast and bacterial leaf blight of rice. Eur J Plant Pathol 152:747–757. https://doi.org/10.1007/s10658-018-1519-3
Jeerapong C, Phupong W, Bangrak P, Intana W, Tuchinda P (2015) Trichoharzianol, a new antifungal from Trichoderma harzianum F031. J Agric Food Chem 63:3704–3708. https://doi.org/10.1021/acs.jafc.5b01258
Ji Z, Ma D, Miao F (2014) Chemical constituents from Trichoderma longibrachiatum, an endophytic fungus derived from marine green alga codium fragile. J Shenyang Univ 26:277–280
Jin X, Custis D (2011) Microencapsulating aerial conidia of Trichoderma harzianum through spray drying at elevated temperatures. Biol Control 56:202–208. https://doi.org/10.1016/j.biocontrol.2010.11.008
Jin X, Harman GE, Taylor AG (1991) Conidial biomass and desiccation tolerance of Trichoderma harzianum produced at different medium water potentials. Biol Control 1:237–243. https://doi.org/10.1016/1049-9644(91)90072-8
Jin-lian C, Kai L, Cui-ping M, Hui-lin G et al (2015) Chemical constituents with siderophores activities from Trichoderma koningiopsis YIM PH30002. Nat Prod Res Dev 27:1878. https://doi.org/10.16333/j.1001-6880.2015.11.008
Jindapunnapat K, Chinnasri B, Kwankuae S (2013) Biological control of root-knot nematodes (Meloidogyne enterolobii) in guava by the fungus Trichoderma harzianum. J Dev Sustain Agric 8:110–118. https://doi.org/10.11178/jdsa.8.110
Jones KA, Burges HD (1998) Technology of formulation and application. In: Formulation of microbial biopesticides: beneficial microorganisms, nematodes and seed treatments. Springer, Dordrecht, pp 7–30
Kachroo A, Robin GP (2013) Systemic signaling during plant defense. Curr Opin Plant Biol 16:527–533. https://doi.org/10.1016/j.pbi.2013.06.019
Kamala T, Indira S (2011) Evaluation of indigenous Trichoderma isolates from Manipur as biocontrol agent against Pythium aphanidermatum on common beans. 3 Biotech 1:217–225. https://doi.org/10.1007/s13205-011-0027-3
Kariuki CK, Mutitu EW, Muiru WM (2020) Effect of Bacillus and Trichoderma species in the management of the bacterial wilt of tomato (Lycopersicum esculentum) in the field. Egypt J Biol Pest Control 30:1–8. https://doi.org/10.1186/s41938-020-00310-4
Karlsson M, Atanasova L, Jensen DF, Zeilinger S (2017) Necrotrophic mycoparasites and their genomes. Microbiol Spectr. https://doi.org/10.1128/microbiolspec.FUNK-0016-2016
Kath J, Dias-Arieira CR, Ferreira JCA, Homiak JA et al (2017) Control of Pratylenchus brachyurus in soybean with Trichoderma spp. and resistance inducers. J Phytopathol 165:791–799. https://doi.org/10.1111/jph.12619
Kawada M, Yoshimoto Y, Kumagai H, Someno T et al (2004) PP2A inhibitors, harzianic acid and related compounds produced by fungus strain F‑1531. J Antibiot 57:235–237. https://doi.org/10.7164/antibiotics.57.235
Keller NP, Turner G, Bennett JW (2005) Fungal secondary metabolism—from biochemistry to genomics. Nat Rev Microbiol 3:937–947. https://doi.org/10.1038/nrmicro1286
Keswani C, Mishra S, Sarma BK, Singh SP, Singh HB (2014) Unraveling the efficient applications of secondary metabolites of various Trichoderma spp. Appl Microbiol Biotechnol 98:533–544. https://doi.org/10.1007/s00253-013-5344-5
Keswani C, Bisen K, Singh V, Sarma BK, Singh HB (2016) Formulation technology of biocontrol agents: present status and future prospects. In: Bioformulations: for sustainable agriculture. Springer, New Delhi, pp 35–52 https://doi.org/10.1007/978-81-322-2779-3_2
Keswani C, Singh HB, Hermosa R, García-Estrada C et al (2019) Antimicrobial secondary metabolites from agriculturally important fungi as next biocontrol agents. Appl Microbiol Biotechnol 103:9287–9303. https://doi.org/10.1007/s00253-019-10209-2
Khan RAA, Najeeb S, Mao Z, Ling J et al (2020) Bioactive secondary metabolites from Trichoderma spp. against phytopathogenic bacteria and root-knot nematode. Microorganisms 8:401. https://doi.org/10.3390/microorganisms8030401
Kiriga AW, Haukeland S, Kariuki GM, Coyne DL, Beek NV (2018) Effect of Trichoderma spp. and Purpureocillium lilacinum on Meloidogyne javanica in commercial pineapple production in Kenya. Biol Control 119:27–32. https://doi.org/10.1016/j.biocontrol.2018.01.005
Kolombet LV, Zhigletsova SK, Kosareva NI, Bystrova EV et al (2008) Development of an extended shelf-life, liquid formulation of the biofungicide Trichoderma asperellum. World J Microbiol Biotechnol 24:123–131. https://doi.org/10.1007/s11274-007-9449-9
Konappa N, Krishnamurthy S, Siddaiah CN, Ramachandrappa NS, Chowdappa S (2018) Evaluation of biological efficacy of Trichoderma asperellum against tomato bacterial wilt caused by Ralstonia solanacearum. Egypt J Biol Pest Control 28:1–11. https://doi.org/10.1186/s41938-018-0069-5
Konappa N, Krishnamurthy S, Arakere UC, Chowdappa S, Ramachandrappa NS (2020) Efficacy of indigenous plant growth-promoting rhizobacteria and Trichoderma strains in eliciting resistance against bacterial wilt in a tomato. Egypt J Biol Pest Control 30:1–13
Kong Z, Jing R, Wu Y, Guo Y et al (2018) Trichodermadiones A and B from the solid culture of Trichoderma atroviride S361, an endophytic fungus in Cephalotaxus fortunei. Fitoterapia 127:362–366. https://doi.org/10.1016/j.fitote.2018.04.004
Kontani M, Sakagami Y, Marumo S (1994) First β‑1,6‑glucan biosynthesis inhibitor, bisvertinolone isolated from fungus, Acremonium strictum and its absolute stereochemistry. Tetrahedron Lett 35:2577–2580. https://doi.org/10.1016/S0040-4039(00)77175-9
Kubicek CP, Herrera-Estrella A, Seidl-Seiboth V, Martinez DA et al (2011) Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol 12:R40. https://doi.org/10.1186/gb-2011-12-4-r40
Kumar P, Chand R (2015) Bio-efficacy of Trichoderma harzianum against root knot nematode Meloidogyne incognita on Brinjal. Ann Plant Prot Sci 23:361–364
Kumar D, Khilari K, Kumar N, Jain SK (2017) Integrated disease management of rice root knot nematode (Meloidogyne graminicola) through organic amendments, Trichoderma spp. and Carbofuran. J Pharmacogn Phytochem 6:2509–2515
Kumar S, Chandra R, Behera L, Keswani C, Sansinenea E (2022) Dual Trichoderma consortium mediated elevation of systemic defense response against early blight in potato. Eur J Plant Pathol 162:681–696. https://doi.org/10.1007/s10658-021-02431-4
Kumar V, Anal AKD, Nath V (2018) Growth response of litchi to arbuscular mycorrhizal co-inoculation with Trichoderma viride, Azotobacter chroococcum and Bacillus megatarium. Indian Phytopathol 71:65–74. https://doi.org/10.1007/s42360-018-0010-6
Lamdan N‑L, Shalaby S, Ziv T, Kenerley CM, Horwitz BA (2015) Secretome of Trichoderma interacting with maize roots: role in induced systemic resistance*[S]. Mol Cell Proteomics 14:1054–1063. https://doi.org/10.1074/mcp.M114.046607
Lang B‑Y, Li J, Zhou X‑X, Chen Y‑H et al (2015) Koninginins L and M, two polyketides from Trichoderma koningii 8662. Phytochem Lett 11:1–4. https://doi.org/10.1016/j.phytol.2014.10.031
Lanlan X, Qiqi Z, He Y, Jingchen W et al (2016) Absolute configuration determination of one new compound trichoderol a from Trichoderma sp. fungus. Chem J Chin Univ 37:1972–1976. https://doi.org/10.7503/cjcu20160499
Le HT, Padgham JL, Sikora RA (2009) Biological control of the rice root-knot nematode Meloidogyne graminicola on rice, using endophytic and rhizosphere fungi. Int J Pest Manag 55:31–36. https://doi.org/10.1080/09670870802450235
Lee S, Behringer G, Hung R, Bennett J (2019) Effects of fungal volatile organic compounds on Arabidopsis thaliana growth and gene expression. Fungal Ecol 37:1–9. https://doi.org/10.1016/j.funeco.2018.08.004
Leggett M, Leland J, Kellar K, Epp B (2011) Formulation of microbial biocontrol agents – an industrial perspective. Can J Plant Pathol 33:101–107. https://doi.org/10.1080/07060661.2011.563050
Leonetti P, Zonno MC, Molinari S, Altomare C (2017) Induction of SA-signaling pathway and ethylene biosynthesis in Trichoderma harzianum-treated tomato plants after infection of the root-knot nematode Meloidogyne incognita. Plant Cell Rep 36:621–631. https://doi.org/10.1007/s00299-017-2109-0
Li B, Li L, Peng Z, Liu D et al (2019) Harzianoic acids A and B, new natural scaffolds with inhibitory effects against hepatitis C virus. Bioorg Med Chem 27:560–567. https://doi.org/10.1016/j.bmc.2018.12.038
Li C‑W, Song R‑Q, Yang L‑B, Deng X (2015) Isolation, purification, and structural identification of an antifungal compound from a Trichoderma strain. J Microbiol Biotechnol 25:1257–1264. https://doi.org/10.4014/jmb.1410.10027
Li D‑L, Chen Y‑C, Tao M‑H, Li H‑H, Zhang W‑M (2012) Two new octahydronaphthalene derivatives from Trichoderma spirale, an endophytic fungus derived from Aquilaria sinensis. Helv Chim Acta 95:805–809. https://doi.org/10.1002/hlca.201100417
Li DL, Chen YC, Li YY, Tao MH, Zhang WM (2010) Isolatjon and identification of anti-tumor constituents from an endophytic fungus of baimuxiang (Aquilaria sinensis). Microbiol. https://doi.org/10.1631/jzus.B1000330
Li G‑H, Zheng L‑J, Liu F‑F, Dang L‑Z et al (2009) New cyclopentenones from strain Trichoderma sp. YLF‑3. Nat Prod Res 23:1431–1435. https://doi.org/10.1080/14786410902843269
Li HY, Luo Y, Zhang XS, Shi WL et al (2014) Trichokonins from Trichoderma pseudokoningii SMF2 induce resistance against Gram-negative Pectobacterium carotovorum subsp. carotovorum in Chinese cabbage. FEMS Microbiol Lett 354:75–82. https://doi.org/10.1111/1574-6968.12427
Li W‑Y, Liu Y, Lin Y‑T, Liu Y‑C et al (2020) Antibacterial harziane diterpenoids from a fungal symbiont Trichoderma atroviride isolated from Colquhounia coccinea var. mollis. Phytochemistry 170:112198. https://doi.org/10.1016/j.phytochem.2019.112198
Li Y, Meng X, Guo D, Gao J et al (2022) A simple and low-cost strategy to improve conidial yield and stress resistance of Trichoderma guizhouense through optimizing illumination conditions. J Fungi 8:50. https://doi.org/10.3390/jof8010050
Liang XR (2016) Secondary metabolites from three marine-derived Trichoderma fungi and their bioactivities. Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai
Liang X‑R, Miao F‑P, Song Y‑P, Liu X‑H, Ji N‑Y (2016) Citrinovirin with a new norditerpene skeleton from the marine algicolous fungus Trichoderma citrinoviride. Bioorganic Med Chem Let 26:5029–5031. https://doi.org/10.1016/j.bmcl.2016.08.093
Lin Y‑R, Lo C‑T, Liu S‑Y, Peng K‑C (2012) Involvement of pachybasin and emodin in self-regulation of Trichoderma harzianum mycoparasitic coiling. J Agric Food Chem 60:2123–2128. https://doi.org/10.1021/jf202773y
Liu X‑H, Hou X‑L, Song Y‑P, Wang B‑G, Ji N‑Y (2020) Cyclonerane sesquiterpenes and an isocoumarin derivative from the marine-alga-endophytic fungus Trichoderma citrinoviride A‑WH-20‑3. Fitoterapia 141:104469. https://doi.org/10.1016/j.fitote.2020.104469
Lo C‑T, Nelson E, Harman GE (1997) Improved biocontrol efficacy of Trichoderma harzianum 1295-22 for foliar phases of turf diseases by use of spray applications. Plant Dis 81:1132–1138. https://doi.org/10.1094/PDIS.1997.81.10.1132
Locatelli GO, dos Santos GF, Botelho PS, Finkler CLL, Bueno LA (2018) Development of Trichoderma sp. formulations in encapsulated granules (CG) and evaluation of conidia shelf-life. Biol Control 117:21–29. https://doi.org/10.1016/j.biocontrol.2017.08.020
López-Bucio J, Pelagio-Flores R, Herrera-Estrella A (2015) Trichoderma as biostimulant: exploiting the multilevel properties of a plant beneficial fungus. Sci Hortic 196:109–123. https://doi.org/10.1016/j.scienta.2015.08.043
López-Mondéjar R, Antón A, Raidl S, Ros M, Pascual JA (2010) Quantification of the biocontrol agent Trichoderma harzianum with real-time TaqMan PCR and its potential extrapolation to the hyphal biomass. Bioresour Technol 101:2888–2891. https://doi.org/10.1016/j.biortech.2009.10.019
Lorito M, Woo SL, Harman GE, Monte E (2010) Translational research on Trichoderma: from omics to the field. Annu Rev Phytopathol 48:395–417. https://doi.org/10.1146/annurev-phyto-073009-114314
de los Santos-Villalobos S, Guzmán-Ortiz DA, Gómez-Lim MA, Délano-Frier JP et al (2013) Potential use of Trichoderma asperellum (Samuels, Liechfeldt et Nirenberg) T8a as a biological control agent against anthracnose in mango (Mangifera indica L.). Biol Control 64:37–44. https://doi.org/10.1016/j.biocontrol.2012.10.006
Lubian C, Kuhn OJ, Portz RL, Agustinha AM, Stangarlin JR (2021) Biological control of Meloidogyne javanica in bean plants by Hohenbuehelia spp. and Trichoderma koningiopsis. Arq Inst Biol. https://doi.org/10.1590/1808-1657000772019
Macías FA, Varela RM, Simonet AM, Cutler HG et al (2000) Bioactive carotanes from Trichoderma virens. J Nat Prod 63:1197–1200. https://doi.org/10.1021/np000121c
Madhavi GB, Bhattiprolu SL, Reddy VB (2011) Compatibility of biocontrol agent Trichoderma viride with various pesticides. J Hortic Sci 6:71–73
Malmierca MG, Cardoza RE, Alexander NJ, McCormick SP et al (2012) Involvement of Trichoderma trichothecenes in the biocontrol activity and induction of plant defense-related genes. Appl Environ Microbiol 78:4856–4868. https://doi.org/10.1128/AEM.00385-12
Malmierca MG, Cardoza RE, Alexander NJ, McCormick SP et al (2013) Relevance of trichothecenes in fungal physiology: disruption of tri5 in Trichoderma arundinaceum. Fungal Genet Biol 53:22–33. https://doi.org/10.1016/j.fgb.2013.02.001
Manzar N, Kashyap AS, Goutam RS, Rajawat MVS et al (2022) Trichoderma: Advent of versatile biocontrol agent, its secrets and insights into mechanism of biocontrol potential. Sustainability 14:12786. https://doi.org/10.3390/su141912786
Martinez C, Blanc F, Le Claire E, Besnard O et al (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. https://doi.org/10.1104/pp.127.1.334
Martínez-Medina A, Van Wees SCM, Pieterse CMJ (2017a) Airborne signals from Trichoderma fungi stimulate iron uptake responses in roots resulting in priming of jasmonic acid-dependent defences in shoots of Arabidopsis thaliana and Solanum lycopersicum. Plant Cell Environ 40:2691–2705. https://doi.org/10.1111/pce.13016
Martínez-Medina A, Fernandez I, Lok GB, Pozo MJ et al (2017b) Shifting from priming of salicylic acid- to jasmonic acid-regulated defences by Trichoderma protects tomato against the root knot nematode Meloidogyne incognita. New Phytol 213:1363–1377. https://doi.org/10.1111/nph.14251
Mastan A, Rane D, Dastager SG, Babu VCS (2021) Molecular insights of fungal endophyte co-inoculation with Trichoderma viride for the augmentation of forskolin biosynthesis in Coleus forskohlii. Phytochemistry 184:112654. https://doi.org/10.1016/j.phytochem.2021.112654
Mathys J, De Cremer K, Timmermans P, Van Kerkhove S et al (2012) Genome-wide characterization of ISR induced in Arabidopsis thaliana by Trichoderma hamatum T382 against Botrytis cinerea infection. Front Plant Sci. https://doi.org/10.3389/fpls.2012.00108
Matsuo H, Noguchi Y, Miyano R, Higo M et al (2020) Thioporidiols A and B: Two new sulfur compounds discovered by molybdenum-catalyzed oxidation screening from Trichoderma polypori FKI-7382. Antibiotics 9:236. https://doi.org/10.3390/antibiotics9050236
Mazzucco CE, Warr G (1996) Trichodimerol (BMS-182123) inhibits lipopolysaccharide-induced eicosanoid secretion in THP‑1 human monocytic cells. J Leukoc Biol 60:271–277. https://doi.org/10.1002/jlb.60.2.271
Mbarga JB, Ten Hoopen GM, Kuat ÚJ, Adiobo A et al (2012) Trichoderma asperellum: A potential biocontrol agent for Pythium myriotylum, causal agent of cocoyam (Xanthosoma sagittifolium) root rot disease in Cameroon. Crop Prot 36:18–22. https://doi.org/10.1016/j.cropro.2012.02.004
Mbarga JB, Begoude BAD, Ambang Z, Meboma M et al (2014) A new oil-based formulation of Trichoderma asperellum for the biological control of cacao black pod disease caused by Phytophthora megakarya. Biol Control 77:15–22. https://doi.org/10.1016/j.biocontrol.2014.06.004
Mbarga JB, Begoude BAD, Ambang Z, Meboma M et al (2020) Field testing an oil-based Trichoderma asperellum formulation for the biological control of cacao black pod disease, caused by Phytophthora megakarya. Crop Prot 132:105134. https://doi.org/10.1016/j.cropro.2020.105134
Mendoza-Mendoza A, Zaid R, Lawry R, Hermosa R et al (2018) Molecular dialogues between Trichoderma and roots: Role of the fungal secretome. Fungal Biol Rev 32:62–85. https://doi.org/10.1016/j.fbr.2017.12.001
Meng J, Cheng W, Heydari H, Wang B et al (2018) Sorbicillinoid-based metabolites from a sponge-derived fungus Trichoderma saturnisporum. Mar Drugs 16:226. https://doi.org/10.3390/md16070226
Meng JJ, Wang B, Cheng W (2017) Study on the secondary metabolites of Trichoderma saturnisporum. Chin J Mar Drugs 36:27–31. https://doi.org/10.3390/metabo9030058
Meyer SL, Massoud SI, Chitwood DJ, Roberts DP (2000) Evaluation of Trichoderma virens and Burkholderia cepacia for antagonistic activity against root-knot nematode, Meloidogyne incognita. Nematology 2:871–879
Miyano R, Matsuo H, Mokudai T, Noguchi Y et al (2020) Trichothioneic acid, a new antioxidant compound produced by the fungal strain Trichoderma virens FKI-7573. J Biosci Bioeng 129:508–513. https://doi.org/10.1016/j.jbiosc.2019.11.007
Mohamed BF, Sallam NM, Alamri SA, Abo-Elyousr KA et al (2020) Approving the biocontrol method of potato wilt caused by Ralstonia solanacearum (Smith) using Enterobacter cloacae PS14 and Trichoderma asperellum T34. Egypt J Biol Pest Control 30:1–13
Morán-Diez E, Hermosa R, Ambrosino P, Cardoza RE et al (2009) The ThPG1 endopolygalacturonase is required for the Trichoderma harzianum—plant beneficial interaction. Mol Plant Microbe Interact 22:1021–1031. https://doi.org/10.1094/mpmi-22-8-1021
Morgan CA, Herman N, White PA, Vesey G (2006) Preservation of micro-organisms by drying; a review. J Microbiol Methods 66:183–193. https://doi.org/10.1016/j.mimet.2006.02.017
Moscatiello R, Sello S, Ruocco M, Barbulova A et al (2018) The Hydrophobin HYTLO1 secreted by the biocontrol fungus Trichoderma longibrachiatum triggers a NAADP-mediated calcium signalling pathway in Lotus japonicus. Int J Mol Sci 19:2596
Motlagh MRS, Jahangiri B, Kulus D, Tymoszuk A, Kaviani B (2022) Endophytic fungi as potential biocontrol agents against Rhizoctonia solani JG Kühn, the causal agent of rice sheath blight disease. Biology 11:1282
Mukherjee AK, Sampath Kumar A, Kranthi S, Mukherjee PK (2014) Biocontrol potential of three novel Trichoderma strains: isolation, evaluation and formulation. 3 Biotech 4:275–281. https://doi.org/10.1007/s13205-013-0150-4
Mukherjee PK, Horwitz BA, Kenerley CM (2012a) Secondary metabolism in Trichoderma – a genomic perspective. Microbiology 158:35–45. https://doi.org/10.1099/mic.0.053629-0
Mukherjee PK, Buensanteai N, Moran-Diez ME, Druzhinina IS, Kenerley CM (2012b) Functional analysis of non-ribosomal peptide synthetases (NRPSs) in Trichoderma virens reveals a polyketide synthase (PKS)/NRPS hybrid enzyme involved in the induced systemic resistance response in maize. Microbiology 158:155–165. https://doi.org/10.1099/mic.0.052159-0
Mukherjee PK, Hurley JF, Taylor JT, Puckhaber L et al (2018) Ferricrocin, the intracellular siderophore of Trichoderma virens, is involved in growth, conidiation, gliotoxin biosynthesis and induction of systemic resistance in maize. Biochem Biophys Res Commun 505:606–611. https://doi.org/10.1016/j.bbrc.2018.09.170
Mukherjee PK, Horwitz BA, Vinale F, Hohmann P et al (2022) Molecular intricacies of Trichoderma-plant-pathogen interactions. Front Fungal Biol. https://doi.org/10.3389/ffunb.2022.892228
Mukhopadhyay R, Kumar D (2020) Trichoderma: a beneficial antifungal agent and insights into its mechanism of biocontrol potential. Egypt J Biol Pest Control 30:133. https://doi.org/10.1186/s41938-020-00333-x
Mukhopadhyay R, Pan S (2012a) Isolation and selection of some antagonistic Trichoderma species from different new alluvial zones of Nadia district, West Bengal. J Bot Soc Bengal 66:149–152
Mukhopadhyay R, Pan S (2012b) Effect of biopriming of radish (Raphanus sativus) seed with some antagonistic isolates of Trichoderma. J Plant Protect Sci 4:46–50
Mukhopadhyay T, Roy K, Sawant S, Deshmukh SK et al (1996) On an unstable antifungal metabolite from Trichoderma koningii isolation and structure elucidation of a new cyclopentenone derivative (3-Dimethylamino-5-hydroxy-5-vinyl-2-cyclopenten-l-one). J Antibiot 49:210–211. https://doi.org/10.7164/antibiotics.49.210
Mukhtar T, Jabbar A, Raja M, Javed H (2018) Management of root-knot nematode, Meloidogyne incognita, in tomato with two Trichoderma species. Pak J Zool 50:1589–1592
Muñoz-Celaya AL, Ortiz-García M, Vernon-Carter EJ, Jauregui-Rincón J et al (2012) Spray-drying microencapsulation of Trichoderma harzianum conidias in carbohydrate polymers matrices. Carbohydr Polym 88:1141–1148. https://doi.org/10.1016/j.carbpol.2011.12.030
Mutawila C, Vinale F, Halleen F, Lorito M, Mostert L (2016) Isolation, production and in vitro effects of the major secondary metabolite produced by Trichoderma species used for the control of grapevine trunk diseases. Plant Pathol 65:104–113. https://doi.org/10.1111/ppa.12385
Nadarajah K, Abdul Rahman NSN (2023) The microbial connection to sustainable agriculture. Plants 12(12):2307. https://doi.org/10.3390/plants12122307
Nafady NA, Sultan R, El-Zawahry AM, Mostafa YS et al (2022) Effective and promising strategy in management of tomato root-knot nematodes by Trichoderma harzianum and arbuscular mycorrhizae. Agronomy 12:315
Nagachandrabose S (2020) Management of potato cyst nematodes using liquid bioformulations of Pseudomonas fluorescens, Purpureocillium lilacinum and Trichoderma viride. Potato Res 63:479–496
Narasimha Murthy K, Nirmala Devi D, Srinivas C (2013) Efficacy of Trichoderma asperellum against Ralstonia solanacearum under greenhouse conditions. Ann Plant Sci 2:342–350
Naserinasab F, Sahebani N, Etebarian HR (2011) Biological control of Meloidogyne javanica by Trichoderma harzianum BI and salicylic acid on tomato. Afr J Food Sci 5:276–280
Natsiopoulos D, Tziolias A, Lagogiannis I, Mantzoukas S, Eliopoulos PA (2022) Growth-promoting and protective effect of Trichoderma atrobrunneum and T. simmonsii on tomato against soil-borne fungal pathogens. Crops 2:202–217. https://doi.org/10.3390/crops2030015
Nautiyal CS, Dion P (2008) Molecular mechanisms of plant and microbe coexistence. Springer
Neelipally RTKR, Anoruo AO, Nelson S (2020) Effect of co-inoculation of Bradyrhizobium and Trichoderma on growth, development, and yield of Arachis hypogaea L. (Peanut). Agronomy 10:1415. https://doi.org/10.3390/agronomy10091415
Ng L, Ngadin A, Azhari M, Zahari N (2015) Potential of Trichoderma spp. as biological control agents against bakanae pathogen (Fusarium fujikuroi) in rice. Asian J Plant Pathol 9:46–58
Nieto-Jacobo MF, Steyaert JM, Salazar-Badillo FB, Nguyen DV et al (2017) Environmental growth conditions of Trichoderma spp. affects indole acetic acid derivatives, volatile organic compounds, and plant growth promotion. Front Plant Sci 8:102. https://doi.org/10.3389/fpls.2017.00102
Nishiyama M, Maeda H, Tonouchi A, Hashimoto M (2019) Neomacrophorin and premacrophorin congeners from Trichoderma sp. 1212-03. Tetrahedron 75:2993–3000. https://doi.org/10.1016/j.tet.2019.04.018
Nogueira-Lopez G, Greenwood DR, Middleditch M, Winefield C et al (2018) The apoplastic secretome of Trichoderma virens during interaction with maize roots shows an inhibition of plant defence and scavenging oxidative stress secreted proteins. Front Plant Sci. https://doi.org/10.3389/fpls.2018.00409
Nuankeaw K, Chaiyosang B, Suebrasri T, Kanokmedhakul S et al (2020) First report of secondary metabolites, Violaceol I and Violaceol II produced by endophytic fungus, Trichoderma polyalthiae and their antimicrobial activity. Mycoscience 61:16–21. https://doi.org/10.1016/j.myc.2019.10.001
Okigbo R, Ikediugwu F (2000) Studies on biological control of postharvest rot in yams (Dioscorea spp.) using Trichoderma viride. J Phytopathol 148:351–355. https://doi.org/10.1046/j.1439-0434.2000.00515.x
Oyekanmi E, Coyne DL, Fagade O, Osonubi O (2007) Improving root-knot nematode management on two soybean genotypes through the application of Bradyrhizobium japonicum, Trichoderma pseudokoningii and Glomus mosseae in full factorial combinations. Crop Prot 26:1006–1012. https://doi.org/10.1016/j.cropro.2006.09.009
Pang X, Lin X, Tian Y, Liang R et al (2018) Three new polyketides from the marine sponge-derived fungus Trichoderma sp. SCSIO41004. Nat Prod Res 32:105–111. https://doi.org/10.1080/14786419.2017.1338286
Parker SR, Cutler HG, Jacyno JM, Hill RA (1997) Biological activity of 6‑pentyl-2 H-pyran-2-one and its analogs. J Agric Food Chem 45:2774–2776. https://doi.org/10.1021/jf960681a
Paul NC, Park S, Liu H, Lee JG et al (2021) Fungi associated with postharvest diseases of sweet potato storage roots and in vitro antagonistic assay of Trichoderma harzianum against the diseases. J Fungi 7:927. https://doi.org/10.3390/jof7110927
Perelló A, Mónaco C, Cordo C (1997) Evaluation of Trichoderma harzianum and Gliocladium roseum in controlling leaf blotch of wheat (Septoria tritici) under in vitro and greenhouse conditions/Auswertung von Trichoderma harzianum und Gliocladium roseum bei der Bekämpfung der Blattfleckenkrankheit an Weizen,(Septoria tritici) unter in vitro und Gewächshausbedingungen. J Plant Dis Protect: 588–598
Perello A, Monaco C, Simon M, Sisterna M, Dal Bello G (2003) Biocontrol efficacy of Trichoderma isolates for tan spot of wheat in Argentina. Crop Prot 22:1099–1106. https://doi.org/10.1016/S0261-2194(03)00143-1
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 416:143–148. https://doi.org/10.1016/S0014-5793(97)01169-1
Poveda J (2021) Insect frass in the development of sustainable agriculture. A review. Agron Sustain Dev 41:5. https://doi.org/10.1007/s13593-020-00656-x
Pradhan PC, Mukhopadhyay A, Kumar R, Patanjali N et al (2022) Performance evaluation of a novel dustable powder formulation of Trichoderma viride for seed treatment against Fusarium wilt in chickpea. Indian Phytopathol 75:1055–1063. https://doi.org/10.1007/s42360-022-00535-3
Prasad R, Rangeshwaran R, Hegde S, Anuroop C (2002) Effect of soil and seed application of Trichoderma harzianum on pigeonpea wilt caused by Fusarium udum under field conditions. Crop Prot 21:293–297. https://doi.org/10.1016/S0261-2194(01)00100-4
Pratap Singh S, Keswani C, Pratap Singh S, Sansinenea E, Xuan Hoat T (2021) Trichoderma spp. mediated induction of systemic defense response in brinjal against Sclerotinia sclerotiorum. Curr Res Microb Sci 2:100051. https://doi.org/10.1016/j.crmicr.2021.100051
Przylucka A, Akcapinar GB, Chenthamara K, Cai F et al (2017) HFB7 – A novel orphan hydrophobin of the Harzianum and Virens clades of Trichoderma, is involved in response to biotic and abiotic stresses. Fungal Genet Biol 102:63–76. https://doi.org/10.1016/j.fgb.2017.01.002
Qaderi S, Safaie N (2023) Endophytic fungi-based wettable powder formulation for Rhizoctonia solani AG‑4 biocontrol. Plant Soil 21:1–7. https://doi.org/10.1007/s11104-023-05987-8
Qian-Cutrone J, Huang S, Chang L‑P, Pirnik DM et al (1996) Harziphilone and fleephilone, two new HIV REV/RRE binding inhibitors produced by Trichoderma harzianum. J Antibiot 49:990–997. https://doi.org/10.7164/antibiotics.49.990
Qin X‑Y, Yang K‑L, Wang C‑Y, Shao C‑L (2014) Secondary metabolites of the zoanthid-derived fungus Trichoderma sp. TA26-28 collected from the South China Sea. Chem Nat Compd 50:961–964. https://doi.org/10.1007/s10600-014-1134-2
Rahman M, Begum M, Alam M (2009) Screening of Trichoderma isolates as a biological control agent against Ceratocystis paradoxa causing pineapple disease of sugarcane. Mycobiology 37:277–285. https://doi.org/10.4489/MYCO.2009.37.4.277
Ranjana JP (2022) Trichoderma spp.: source of secondary metabolites. Vigyan Varta 3:97–100
Rao M (2007) Papaya seedlings colonized by the bio-agents Trichoderma harzianum and Pseudomonas fluorescens to control root-knot nematodes. Nematol Mediterr
Reddy PP, Rao M, Nagesh M (1996) Management of citrus nematode, Tylenchulus semipenetrans, by integration of Trichoderma harzianum with oil cakes. Nematol Mediterr 24:265–267
Rippa S, Eid M, Formaggio F, Toniolo C, Béven L (2010) Hypersensitive-like response to the pore-former peptaibol alamethicin in Arabidopsis thaliana. Chem Bio Chem 11:2042–2049. https://doi.org/10.1002/cbic.201000262
Rivera-Chávez J, Raja HA, Graf TN, Gallagher JM et al (2017) Prealamethicin F50 and related peptaibols from Trichoderma arundinaceum: Validation of their authenticity via in situ chemical analysis. RSC Adv 7:45733–45741. https://doi.org/10.1039/C7RA09602J
Rivera-Méndez W, Obregón M, Morán-Diez ME, Hermosa R, Monte E (2020) Trichoderma asperellum biocontrol activity and induction of systemic defenses against Sclerotium cepivorum in onion plants under tropical climate conditions. Biol Control 141:104145. https://doi.org/10.1016/j.biocontrol.2019.104145
Roberts DP, Maul JE, McKenna LF, Emche SE et al (2010) Selection of genetically diverse Trichoderma spp. isolates for suppression of Phytophthora capsici on bell pepper. Can J Microbiol 56:864–873. https://doi.org/10.1139/w10-071
Rojo FG, Reynoso MM, Ferez M, Chulze SN, Torres AM (2007) Biological control by Trichoderma species of Fusarium solani causing peanut brown root rot under field conditions. Crop Prot 26:549–555. https://doi.org/10.1016/j.cropro.2006.05.006
Ron M, Kantety R, Martin G, Avidan N et al (2000) High-resolution linkage analysis and physical characterization of the EIX-responding locus in tomato. Theor Appl Genet 100:184. https://doi.org/10.1007/s001220050025
Rosado IV, Rey M, Codón AC, Govantes J et al (2007) QID74 Cell wall protein of Trichoderma harzianum is involved in cell protection and adherence to hydrophobic surfaces. Fungal Genet Biol 44:950–964. https://doi.org/10.1016/j.fgb.2007.01.001
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. https://doi.org/10.1046/j.1365-313X.2002.01490.x
Rudresh DL, Shivaprakash MK, Prasad RD (2005) Tricalcium phosphate solubilizing abilities of Trichoderma spp. in relation to P uptake and growth and yield parameters of chickpea (Cicer arietinum L.). Can J Microbiol 51:217–222. https://doi.org/10.1139/w04-127
Ruocco M, Lanzuise S, Lombardi N, Woo SL et al (2015) Multiple roles and effects of a novel Trichoderma hydrophobin. Mol Plant Microbe Interact 28:167–179. https://doi.org/10.1094/mpmi-07-14-0194-r
Sáenz-Mata J, Jiménez-Bremont JF (2012) HR4 gene is induced in the Arabidopsis-Trichoderma atroviride beneficial interaction. Int J Mol Sci 13:9110–9128. https://doi.org/10.3390/ijms13079110
Sahebani N, Hadavi N (2008) Biological control of the root-knot nematode Meloidogyne javanica by Trichoderma harzianum. Soil Biol Biochem 40:2016–2020. https://doi.org/10.1016/j.soilbio.2008.03.011
Salas-Marina MA, Isordia-Jasso MI, Islas-Osuna MA, Delgado-Sánchez P et al (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. https://doi.org/10.3389/fpls.2015.00077
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. https://doi.org/10.1099/mic.0.053140-0
Sánchez-Montesinos B, Diánez F, Moreno-Gavira A, Gea FJ, Santos M (2019) Plant growth promotion and biocontrol of Pythium ultimum by saline tolerant Trichoderma isolates under salinity stress. Int J Environ Res Public Health 16:2053. https://doi.org/10.3390/ijerph16112053
Saravanakumar K, Fan L, Fu K, Yu C et al (2016) Cellulase from Trichoderma harzianum interacts with roots and triggers induced systemic resistance to foliar disease in maize. Sci Rep 6:35543. https://doi.org/10.1038/srep35543
Saravanakumar K, Li Y, Yu C, Q‑q W et al (2017) Effect of Trichoderma harzianum on maize rhizosphere microbiome and biocontrol of Fusarium Stalk rot. Sci Rep 7:1–13. https://doi.org/10.1038/s41598-017-01680-w
Saravanakumar K, Mandava S, Chellia R, Jeevithan E et al (2019) Novel metabolites from Trichoderma atroviride against human prostate cancer cells and their inhibitory effect on Helicobacter pylori and Shigella toxin producing Escherichia coli. Microb Pathog 126:19–26. https://doi.org/10.1016/j.micpath.2018.10.011
Sayed M, Abdel-rahman T, Ragab A, Abdellatif A (2019) Biocontrol of root-knot nematode Meloidogyne incognita by chitinolytic Trichoderma spp. Egypt J Agron 18:30–47. https://doi.org/10.21608/EJAJ.2019.52842
Schisler DA, Slininger PJ, Behle RW, Jackson MA (2004) Formulation of Bacillus spp. for biological control of plant diseases. Phytopathology® 94:1267–1271. https://doi.org/10.1094/phyto.2004.94.11.1267
Schlaeppi K, Bulgarelli D (2015) The plant microbiome at work. Mol Plant Microbe Interact 28:212–217. https://doi.org/10.1094/mpmi-10-14-0334-fi
Schuster A, Schmoll M (2010) Biology and biotechnology of Trichoderma. Appl Microbiol Biotechnol 87:787–799. https://doi.org/10.1007/s00253-010-2632-1
Segarra G, Casanova E, Avilés M, Trillas I (2010) Trichoderma asperellum strain T34 controls Fusarium wilt disease in tomato plants in soilless culture through competition for iron. Microb Ecol 59:141–149. https://doi.org/10.1007/s00248-009-9545-5
Seidl-Seiboth V, Gruber S, Sezerman U, Schwecke T et al (2011) Novel hydrophobins from Trichoderma define a new hydrophobin subclass: Protein properties, evolution, regulation and processing. J Mol Evol 72:339–351. https://doi.org/10.1007/s00239-011-9438-3
Shahriar SA, Islam MN, Chun CNW, Kaur P et al (2022) Microbial metabolomics interaction and ecological challenges of Trichoderma species as biocontrol inoculant in crop rhizosphere. Agronomy 12:900. https://doi.org/10.3390/agronomy12040900
Sharma A, Salwan R, Sharma V (2022) Extracellular proteins of Trichoderma and their role in plant health. S Afr J Bot 147:359–369. https://doi.org/10.1016/j.sajb.2022.01.036
Sharon E, Bar-Eyal M, Chet I, Herrera-Estrella A et al (2001) Biological control of the root-knot nematode Meloidogyne javanica by Trichoderma harzianum. Phytopathology® 91:687–693. https://doi.org/10.1016/j.soilbio.2008.03.011
Shashikumar H, Koulagi S, Navyashree S (2019) Compatibility of Trichoderma viride and Trichoderma harzianum with fungicides against soil borne diseases of tomato and cabbage. Int J Curr Microbiol Appl Sci 8:1920–1928. https://doi.org/10.20546/ijcmas.2019.804.225
Shentu X, Zhan X, Ma Z, Yu X, Zhang C (2014) Antifungal activity of metabolites of the endophytic fungus Trichoderma brevicompactum from garlic. Braz J Microbiol 45:248–254. https://doi.org/10.1590/S1517-83822014005000036
Shi Z (2018) Chemical structures and biological activities of secondary metabolites from five marine-alga-epiphytic fungi. Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai
Shi T, Shao C‑L, Liu Y, Zhao D‑L et al (2020a) Terpenoids from the coral-derived fungus Trichoderma harzianum (XS-20090075) induced by chemical epigenetic manipulation. Front Microbiol 11:572. https://doi.org/10.3389/fmicb.2020.00572
Shi W‑L, Chen X‑L, Wang L‑X, Gong Z‑T et al (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 67:2191–2205. https://doi.org/10.1093/jxb/erw023
Shi X‑S, Wang D‑J, Li X‑M, Li H‑L et al (2017) Antimicrobial polyketides from Trichoderma koningiopsis QA‑3, an endophytic fungus obtained from the medicinal plant Artemisia argyi. RSC Adv 7:51335–51342. https://doi.org/10.1039/C7RA11122C
Shi Z‑Z, Fang S‑T, Miao F‑P, Yin X‑L, Ji N‑Y (2018a) Trichocarotins A–H and trichocadinin A, nine sesquiterpenes from the marine-alga-epiphytic fungus Trichoderma virens. Bioorg Chem 81:319–325. https://doi.org/10.1016/j.bioorg.2018.08.027
Shi Z‑Z, Miao F‑P, Fang S‑T, Yin X‑L, Ji N‑Y (2018b) Sulfurated diketopiperazines from an algicolous isolate of Trichoderma virens. Phytochem Lett 27:101–104. https://doi.org/10.1016/j.phytol.2018.07.005
Shi Z‑Z, Liu X‑H, Li X‑N, Ji N‑Y (2020b) Antifungal and antimicroalgal trichothecene sesquiterpenes from the marine algicolous fungus Trichoderma brevicompactum A‑DL-9‑2. J Agric Food Chem 68:15440–15448. https://doi.org/10.1021/acs.jafc.0c05586
Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43. https://doi.org/10.1146/annurev-phyto-073009-114450
Siddiqui IA, Amer Zareen M, Javad Zaki M, Shaukat S (2001) Use of Trichoderma species in the control of Meloidogyne javaniva, root-knot nematode in the okra and mungbean. Pak J Biol Sci 4:846–848. https://doi.org/10.3923/pjbs.2001.846.848
Singh E, Chandra P (2019) Fungal community for novel secondary metabolites. In: Perspective for Value-Added Products and Environments. Recent advancement in white biotechnology through fungi, vol 2. Springer, Cham, pp 249–283 https://doi.org/10.1007/978-3-030-14846-1
Singh H, Singh BN, Singh S, Sarma B (2013) Exploring different avenues of Trichoderma as a potent bio-fungicidal and plant growth promoting candidate-an overview. Ann Rev Plant Pathol 5:315–321
Singh J, Khilari K, Singh R, Mishra P et al (2019) Studies on the compatibility of Trichoderma spp. with nematicides under in vitro conditions. J Pharmacogn Phytochem 8:8–11
Singh S, Dureja P, Tanwar R, Singh A (2005) Production and antifungal activity of secondary metabolites of Trichoderma virens. Pestic Res J 17:26–29
Sivakumar D, Wijeratnam RW, Wijesundera R, Marikar F, Abeyesekere M (2000) Antagonistic effect of Trichoderma harzianum on postharvest pathogens of rambutan (Nephelium lappaceum). Phytoparasitica 28:240–247. https://doi.org/10.1007/BF02981802
Solanki MK, Singh N, Singh RK, Singh P et al (2011) Plant defense activation and management of tomato root rot by a chitin-fortified Trichoderma/Hypocrea formulation. Phytoparasitica 39:471–481. https://doi.org/10.1007/s12600-011-0188-y
Song F, Dai H, Tong Y, Ren B et al (2010) Trichodermaketones A–D and 7‑O-Methylkoninginin D from the marine fungus Trichoderma koningii. J Nat Prod 73:806–810. https://doi.org/10.1021/np900642p
Song Y, Miao F, Yin X, Ji N (2020) Three nitrogen-containing metabolites from an algicolous isolate of Trichoderma asperellum. Mar Life Sci Technol 2:155–160. https://doi.org/10.1007/s42995-020-00030-6
Song Y‑P, Fang S‑T, Miao F‑P, Yin X‑L, Ji N‑Y (2018a) Diterpenes and sesquiterpenes from the marine algicolous fungus Trichoderma harzianum X‑5. J Nat Prod 81:2553–2559. https://doi.org/10.1021/acs.jnatprod.8b00714
Song Y‑P, Miao F‑P, Fang S‑T, Yin X‑L, Ji N‑Y (2018b) Halogenated and nonhalogenated metabolites from the marine-alga-endophytic fungus Trichoderma asperellum cf44‑2. Mar Drugs 16:266. https://doi.org/10.3390/md16080266
Sood M, Kapoor D, Kumar V, Sheteiwy MS et al (2020) Trichoderma: The “secrets” of a multitalented biocontrol agent. Plants 9:762. https://doi.org/10.3390/plants9060762
Sriram N, Kalayarasan S, Sudhandiran G (2009) Epigallocatechin-3-gallate exhibits anti-fibrotic effect by attenuating bleomycin-induced glycoconjugates, lysosomal hydrolases and ultrastructural changes in rat model pulmonary fibrosis. Chem Biol Interact 180:271–280. https://doi.org/10.1016/j.cbi.2009.02.017
Sriram S, Roopa KP, Savitha MJ (2011) Extended shelf-life of liquid fermentation derived talc formulations of Trichoderma harzianum with the addition of glycerol in the production medium. Crop Prot 30:1334–1339. https://doi.org/10.1016/j.cropro.2011.06.003
Stewart A, Hill R (2014) Applications of Trichoderma in plant growth promotion. In: Biotechnology and biology of Trichoderma. Elsevier, Amsterdam, pp 415–428 https://doi.org/10.1016/B978-0-444-59576-8.00031-X
Steyaert JM, Ridgway HJ, Elad Y, Stewart A (2003) Genetic basis of mycoparasitism: a mechanism of biological control by species of Trichoderma. N Z J Crop Hortic Sci 31:281–291. https://doi.org/10.1080/01140671.2003.9514263
Stummer BE, Zhang X, Yang H, Harvey PR (2022) Co-inoculation of Trichoderma gamsii A5MH and Trichoderma harzianum Tr906 in wheat suppresses in planta abundance of the crown rot pathogen Fusarium pseudograminearum and impacts the rhizosphere soil fungal microbiome. Biol Control 165:104809. https://doi.org/10.1016/j.biocontrol.2021.104809
Sulaiman MM, Yass ST, Aish AA, Basheer L, Yasir SJ, Youssef SA (2020) Activity of Trichoderma spp. against Erwinia carotovora causal agent of potato tuber soft rot. Plant Arch 20:115–8.
Suman J, Rakshit A, Ogireddy SD, Singh S et al (2022) Microbiome as a key player in sustainable agriculture and human health. Front Soil Sci 2:821589. https://doi.org/10.3389/fsoil.2022.821589
Sundaramoorthy S, Balabaskar P (2013) Biocontrol efficacy of Trichoderma spp. against wilt of tomato caused by Fusarium oxysporum f. sp. lycopersici. J Appl Biol Biotechnol 1:36–40. https://doi.org/10.7324/JABB.2013.1306
Suprapta DN (2012) Potential of microbial antagonists as biocontrol agents against plant fungal pathogens. J ISSAAS 18:1–8
Szabó M, Csepregi K, Gálber M, Virányi F, Fekete C (2012) Control plant-parasitic nematodes with Trichoderma species and nematode-trapping fungi: The role of chi18‑5 and chi18-12 genes in nematode egg-parasitism. Biol Control 63:121–128. https://doi.org/10.1016/j.biocontrol.2012.06.013
Szabó M, Urbán P, Virányi F, Kredics L, Fekete C (2013) Comparative gene expression profiles of Trichoderma harzianum proteases during in vitro nematode egg-parasitism. Biol Control 67:337–343. https://doi.org/10.1016/j.biocontrol.2013.09.002
Tamura A, Kotani H, Naruto S (1975) Trichoviridin and dermadin from Trichoderma sp. TK‑1. J Antibiot 28:161–162. https://doi.org/10.7164/antibiotics.28.161
TariqJaveed M, Farooq T, Al-Hazmi AS, Hussain MD, Rehman AU (2021) Role of Trichoderma as a biocontrol agent (BCA) of phytoparasitic nematodes and plant growth inducer. J Invertebr Pathol 183:107626. https://doi.org/10.1016/j.jip.2021.107626
Tarus P, Lang’at-Thoruwa C, Wanyonyi A, Chhabra S (2003) Bioactive metabolites from Trichoderma harzianum and Trichoderma longibrachiatum. Bull Chem Soc Ethiop 17:185–190. https://doi.org/10.4314/bcse.v17i2.61675
Thambugala KM, Daranagama DA, Phillips AJL, Kannangara SD, Promputtha I (2020) Fungi vs. fungi in biocontrol: an overview of fungal antagonists applied against fungal plant pathogens. Front Cell Infect Microbiol 10:604923. https://doi.org/10.3389/fcimb.2020.604923
Tyśkiewicz R, Nowak A, Ozimek E, Jaroszuk-Ściseł J (2022) Trichoderma: the current status of its application in agriculture for the biocontrol of fungal phytopathogens and stimulation of plant growth. Int J Mol Sci 23:2329
Ubalua A, Oti E (2007) Antagonistic properties of Trichoderma viride on post harvest cassava root rot pathogens. Afr J Biotechnol. https://doi.org/10.3390/ijms23042329
Utkhede R, Koch C (2004) Biological treatments to control bacterial canker of greenhouse tomatoes. BioControl 49:305–313. https://doi.org/10.1023/B:BICO.0000025373.69584.08
Valenzuela NL, Angel DN, Ortiz DT, Rosas RA et al (2015) Biological control of anthracnose by postharvest application of Trichoderma spp. on maradol papaya fruit. BioControl 91:88–93. https://doi.org/10.1016/j.biocontrol.2015.08.002
Van Wees SCM, Van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448. https://doi.org/10.1016/j.pbi.2008.05.005
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. https://doi.org/10.1104/pp.109.141291
Verma M, Brar SK, Tyagi R, Surampalli R, Valero J (2007) Antagonistic fungi, Trichoderma spp.: panoply of biological control. Biochem Eng J 37:1–20. https://doi.org/10.1016/j.bej.2007.05.012
Vicente MF, Cabello A, Platas G, Basilio A et al (2001) Antimicrobial activity of ergokonin A from Trichoderma longibrachiatum. J Appl Microbiol 91:806–813. https://doi.org/10.1046/j.1365-2672.2001.01447.x
Vinale F, Sivasithamparam K (2020) Beneficial effects of Trichoderma secondary metabolites on crops. Phytother Res 34:2835–2842. https://doi.org/10.1002/ptr.6728
Vinale F, Marra R, Scala F, Ghisalberti EL et al (2006) Major secondary metabolites produced by two commercial Trichoderma strains active against different phytopathogens. Lett Appl Microbiol 43:143–148. https://doi.org/10.1111/j.1472-765X.2006.01939.x
Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R et al (2008a) Trichoderma-plant-pathogen interactions. Soil Biol Biochem 40:1–10. https://doi.org/10.1016/j.soilbio.2007.07.002
Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R et al (2008b) A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiol Mol Plant Pathol 72:80–86. https://doi.org/10.1016/j.pmpp.2008.05.005
Vinale F, Flematti G, Sivasithamparam K, Lorito M et al (2009a) Harzianic acid, an antifungal and plant growth promoting metabolite from Trichoderma harzianum. J Nat Prod 72:2032–2035. https://doi.org/10.1021/np900548p
Vinale F, Ghisalberti EL, Sivasithamparam K, Marra R et al (2009b) Factors affecting the production of Trichoderma harzianum secondary metabolites during the interaction with different plant pathogens. Lett Appl Microbiol 48:705–711. https://doi.org/10.1111/j.1472-765X.2009.02599.x
Vinale F, Sivasithamparam K, Ghisalberti EL, Ruocco M et al (2012) Trichoderma secondary metabolites that affect plant metabolism. Nat Prod Commun 7:1545–1550. https://doi.org/10.1177/1934578X1200701133
Vinale F, Nigro M, Sivasithamparam K, Flematti G et al (2013) Harzianic acid: a novel siderophore from Trichoderma harzianum. FEMS Microbiol Lett 347:123–129. https://doi.org/10.1111/1574-6968.12231
Vinale F, Manganiello G, Nigro M, Mazzei P et al (2014) A novel fungal metabolite with beneficial properties for agricultural applications. Molecules 19:9760–9772. https://doi.org/10.3390/molecules19079760
Vinale F, Strakowska J, Mazzei P, Piccolo A et al (2016) Cremenolide, a new antifungal, 10-member lactone from Trichoderma cremeum with plant growth promotion activity. Nat Prod Res 30:2575–2581. https://doi.org/10.1080/14786419.2015.1131985
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. https://doi.org/10.1111/j.1364-3703.2006.00335.x
Viterbo A, Horwitz BA (2010) Mycoparasitism. In: Cellular and molecular biology of filamentous fungi, pp 676–693 https://doi.org/10.1128/9781555816636
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. https://doi.org/10.1111/j.1364-3703.2007.00430.x
Viterbo A, Landau U, Kim S, Chernin L, Chet I (2010) Characterization of ACC deaminase from the biocontrol and plant growth-promoting agent Trichoderma asperellum T203. FEMS Microbiol Lett 305:42–48. https://doi.org/10.1111/j.1574-6968.2010.01910.x
Wang C, Zolotarskaya OY, Nair SS, Ehrhardt CJ et al (2016) Real-Time observation of antimicrobial polycation effects on Escherichia coli: Adapting the carpet model for membrane disruption to quaternary copolyoxetanes. Langmuir 32:2975–2984. https://doi.org/10.1021/acs.langmuir.5b04247
Wang Z, Li Y, Zhuang L, Yu Y et al (2019) A rhizosphere-derived consortium of Bacillus subtilis and Trichoderma harzianum suppresses common scab of potato and increases yield. Comput Struct Biotechnol J 17:645–653. https://doi.org/10.1016/j.csbj.2019.05.003
Weindling R (1932) Trichoderma lignorum as a parasite of other soil fungi. Phytopathology 22:837–845
Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511. https://doi.org/10.1093/jexbot/52.suppl_1.487
Woo SL, Hermosa R, Lorito M, Monte E (2023) Trichoderma: a multipurpose, plant-beneficial microorganism for eco-sustainable agriculture. Nat Rev Microbiol 21:312–326. https://doi.org/10.1038/s41579-022-00819-5
Wu B, Oesker V, Wiese J, Schmaljohann R, Imhoff JF (2014) Two new antibiotic pyridones produced by a marine fungus, Trichoderma sp. strain MF106. Mar Drugs 12:1208–1219. https://doi.org/10.3390/md12031208
Wu Y‑W, Ouyang J, Xiao X‑H, Gao W‑Y, Liu Y (2006) Antimicrobial properties and toxicity of anthraquinones by microcalorimetric bioassay. Chin J Chem 24:45–50. https://doi.org/10.1002/cjoc.200690020
Xiao-Yan S, Qing-Tao S, Shu-Tao X, Xiu-Lan C et al (2006) Broad-spectrum antimicrobial activity and high stability of Trichokonins from Trichoderma koningii SMF2 against plant pathogens. FEMS Microbiol Lett 260:119–125. https://doi.org/10.1111/j.1574-6968.2006.00316.x
Xie Z‑L, Li H‑J, Wang L‑Y, Liang W‑L et al (2013) Trichodermaerin, a new diterpenoid lactone from the marine fungus Trichoderma erinaceum associated with the sea star Acanthaster planci. Nat Prod Commun 8:67–68. https://doi.org/10.1177/1934578X1300800116
Xuan Q‑C, Huang R, Chen Y‑W, Miao C‑P et al (2014a) Cyclonerol derivatives from Trichoderma longibrachiatum YM311505. Nat Prod Commun. https://doi.org/10.1177/1934578X1400900307
Xuan Q‑C, Huang R, Miao C‑P, Chen Y‑W et al (2014b) Secondary metabolites of endophytic fungus Trichoderma sp. YM 311505 of Azadirachta indica. Chem Nat Compound 50:139–141. https://doi.org/10.1007/s10600-014-0891-2
Yamazaki H, Saito R, Takahashi O, Kirikoshi R et al (2015) Trichoketides A and B, two new protein tyrosine phosphatase 1B inhibitors from the marine-derived fungus Trichoderma sp. J Antibiot 68:628–632. https://doi.org/10.1038/ja.2015.44
Yamazaki H, Yagi A, Takahashi O, Yamaguchi Y et al (2020a) Antifungal trichothecene sesquiterpenes obtained from the culture broth of marine-derived Trichoderma cf. brevicompactum and their structure-activity relationship. Bioorganic Med Chem Lett 30:127375. https://doi.org/10.1016/j.bmcl.2020.127375
Yamazaki H, Takahashi O, Kirikoshi R, Yagi A et al (2020b) Epipolythiodiketopiperazine and trichothecene derivatives from the NaI-containing fermentation of marine-derived Trichoderma cf. brevicompactum. J Antibiot 73:559–567. https://doi.org/10.1038/s41429-020-0314-5
Yan L, Khan RAA (2021) Biological control of bacterial wilt in tomato through the metabolites produced by the biocontrol fungus, Trichoderma harzianum. Egypt J Biol Pest Control 31:1–9. https://doi.org/10.1186/s41938-020-00351-9
Yang C‑A, Cheng C‑H, Lo C‑T, Liu S‑Y et al (2011) A novel l‑amino acid oxidase from Trichoderma harzianum ETS 323 associated with antagonism of Rhizoctonia solani. J Agric Food Chem 59:4519–4526. https://doi.org/10.1021/jf104603w
Yang Z‑S, Li G‑H, Zhao P‑J, Zheng X et al (2010) Nematicidal activity of Trichoderma spp. and isolation of an active compound. World J Microbiol Biotechnol 26:2297–2302. https://doi.org/10.1007/s11274-010-0410-y
Yao X, Guo H, Zhang K, Zhao M et al (2023) Trichoderma and its role in biological control of plant fungal and nematode disease. Front Microbiol 14:1160551. https://doi.org/10.3389/fmicb.2023.1160551
Yedidia I, Shoresh M, Kerem Z, Benhamou N et al (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. https://doi.org/10.1128/AEM.69.12.7343-7353.2003
Yendyo S, Ramesh G, Pandey BR (2017) Evaluation of Trichoderma spp., Pseudomonas fluorescens and Bacillus subtilis for biological control of Ralstonia wilt of tomato. F1000Res. https://doi.org/10.12688/f1000research.12448.3
Yin M, Fasoyin OE, Wang C, Yue Q et al (2020) Herbicidal efficacy of harzianums produced by the biofertilizer fungus, Trichoderma brevicompactum. AMB Expr 10:118. https://doi.org/10.1186/s13568-020-01055-x
You J, Dai H, Chen Z, Liu G et al (2010) Trichoderone, a novel cytotoxic cyclopentenone and cholesta‑7, 22-diene-3β, 5α, 6β-triol, with new activities from the marine-derived fungus Trichoderma sp. J Ind Microbiol Biotechnol 37:245–252. https://doi.org/10.1007/s10295-009-0667-z
Yu J‑Y, Shi T, Zhou Y, Xu Y et al (2021) Naphthalene derivatives and halogenate quinoline from the coral-derived fungus Trichoderma harzianum (XS-20090075) through OSMAC approach. J Asian Nat Prod Res 23:250–257. https://doi.org/10.1080/10286020.2020.1729752
Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant Microbe Interact 25:139–150. https://doi.org/10.1094/mpmi-06-11-0179
Zhang L, Zhang J (2015) Isolation and purification of active compound from Trichoderma viridescens and its inhibitory activities against phytopathogens. Sci Agric Sin 48:882–888. https://doi.org/10.3864/j.issn.0578-1752.2015.05.06
Zhang L, Niaz SI, Khan D, Wang Z et al (2017b) Induction of diverse bioactive secondary metabolites from the mangrove endophytic fungus Trichoderma sp. (strain 307) by co-cultivation with Acinetobacter johnsonii (strain B2). Mar Drugs 15:35. https://doi.org/10.3390/md15020035
Zhang M, Li N, Chen R, Zou J, Wang C (2014a) Two terpenoids and a polyketide from the endophytic fungus Trichoderma sp. Xy24 isolated from mangrove plant Xylocarpus granatum. J Chin Pharm Sci 23:421–424. https://doi.org/10.5246/jcps.2014.06.056
Zhang M, Liu J‑M, Zhao J‑L, Li N et al (2016) Two new diterpenoids from the endophytic fungus Trichoderma sp. Xy24 isolated from mangrove plant Xylocarpus granatum. Chin Chem Lett 27:957–960. https://doi.org/10.1016/j.cclet.2016.02.008
Zhang Q‑Q, Chen L, Hu X, Gong M‑W et al (2014b) Novel cytotoxic metabolites from the marine-derived fungus Trichoderma citrinoviride. Heterocycles 89:189. https://doi.org/10.3987/COM-13-12874
Zhang S, Gan Y, Xu B (2014c) Efficacy of Trichoderma longibrachiatum in the control of Heterodera avenae. BioControl 59:319–331. https://doi.org/10.1007/s10526-014-9566-y
Zhang S, Gan Y, Ji W, Xu B, Hou B, Liu J (2017) Mechanisms and characterization of Trichoderma longibrachiatum T6 in suppressing nematodes (Heterodera avenae) in wheat. Front Plant Sci 8:1491. https://doi.org/10.3389/fpls.2017.01491
Zhang S, Gan Y, Ji W, Xu B et al (2017c) Mechanisms and characterization of Trichoderma longibrachiatum T6 in suppressing nematodes (Heterodera avenae) in wheat. Front Plant Sci 8:1491. https://doi.org/10.3389/fpls.2017.01491
Zhang S, Sun F, Liu L, Bao L et al (2020a) Dragonfly-Associated Trichoderma harzianum QTYC77 is not only a potential biological control agent of Fusarium oxysporum f. sp. cucumerinum but also a source of new antibacterial agents. J Agric Food Chem 68:14161–14167. https://doi.org/10.1021/acs.jafc.0c05760
Zhang Y, Tian C, Xiao J, Wei L et al (2020b) Soil inoculation of Trichoderma asperellum M45a regulates rhizosphere microbes and triggers watermelon resistance to Fusarium wilt. AMB Expr 10:1–13. https://doi.org/10.1186/s13568-020-01126-z
Zhao D‑L, Yang L‑J, Shi T, Wang C‑Y et al (2019) Potent phytotoxic harziane diterpenes from a soft coral-derived strain of the fungus Trichoderma harzianum XS-20090075. Sci Rep 9:1–9. https://doi.org/10.1038/s41598-019-49778-7
Zhao D‑L, Zhang X‑F, Huang R‑H, Wang D et al (2020) Antifungal nafuredin and epithiodiketopiperazine derivatives from the mangrove-derived fungus Trichoderma harzianum D13. Front Microbiol 11:1495. https://doi.org/10.3389/fmicb.2020.01495
Zhao R, Mao LJ, Zhang CL (2023) Three new species of Trichoderma (Hypocreales, Hypocreaceae) from soils in China. MycoKeys 97:21–40. https://doi.org/10.3897/mycokeys.97.101635
Zheng C‑J, Sun P‑X, Jin G‑L, Qin L‑P (2011) Sesquiterpenoids from Trichoderma atroviride, an endophytic fungus in Cephalotaxus fortunei. Fitoterapia 82:1035–1038. https://doi.org/10.1016/j.fitote.2011.06.010
Zhou P, Wu Z, Tan D, Yang J et al (2017) Atrichodermones A–C, three new secondary metabolites from the solid culture of an endophytic fungal strain, Trichoderma atroviride. Fitoterapia 123:18–22. https://doi.org/10.1016/j.fitote.2017.09.012
Zhou X‑X, Li J, Yang Y‑H, Zeng Y, Zhao P‑J (2014) Three new koninginins from Trichoderma neokongii 8722. Phytochem Lett 8:137–140. https://doi.org/10.1016/j.phytol.2014.03.004
Zhou Y, Yang L, Wang J, Guo L, Huang J (2021) Synergistic effect between Trichoderma virens and Bacillus velezensis on the control of tomato bacterial wilt disease. Hortic 7:439. https://doi.org/10.3390/horticulturae7110439
Zou J‑X, Song Y‑P, Ji N‑Y (2021) Deoxytrichodermaerin, a harziane lactone from the marine algicolous fungus Trichoderma longibrachiatum A‑WH-20‑2. Nat Prod Res 35:216–221. https://doi.org/10.1080/14786419.2019.1622110
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Alizadeh, M., Qaderi, S., Roshanroo, M. et al. Contouring Multifaceted Biological Activities and Applications of Trichoderma spp. for Managing Plant Health. Journal of Crop Health (2024). https://doi.org/10.1007/s10343-024-00976-y
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DOI: https://doi.org/10.1007/s10343-024-00976-y