Advertisement

Trichoderma: A Multifaceted Fungus for Sustainable Agriculture

  • Swati Sachdev
  • Rana Pratap Singh
Chapter
  • 44 Downloads

Abstract

Sustainable agricultural practices are keys for food security of the world’s burgeoning population. Trichoderma is a ubiquitous fungus that offers several avenues for sustainable agriculture. The panoply of mechanisms displayed by several species of Trichoderma makes them a better solution for conventional agricultural problems. Plant protection from unfavorable biotic and abiotic conditions under circumstances of changing global climatic scenario and promoting their growth in soil with limited or poor nutrient conditions are marvelous attributes of Trichoderma. Understanding the mechanisms such as the function of secondary metabolites and cell wall degrading enzymes in mycoparasitism and antibiosis, pathways triggered for induced systemic resistance and enhanced nutrient use efficiency displayed by different strains of Trichoderma at the physiological, biochemical, and molecular level are essential for harnessing their potential efficiently. Gathering information on performances of Trichoderma spp. under variable environmental conditions and their vigilant amalgamation for selection of strains with multiple activity and/or development of consortia for formulation of successful product is the need for current agriculture scenario. The current chapter made an effort to compile information on the beneficial role and mechanisms involved by strains of Trichoderma at different levels to enhance knowledge for exploring future research opportunities.

Keywords

Antibiosis Consortia Induced systemic resistance Mycoparasitism Nutrient use efficiency Sustainable agriculture 

Notes

Acknowledgement

The authors gratefully acknowledge University Grant Commission, New Delhi, India, for providing UGC-Senior Research Fellowship grant as financial support to Swati Sachdev.

Conflict of Interest

The authors declare no conflict of interest.

References

  1. Abbas A, Jiang D, Fu Y (2017) Trichoderma spp. as antagonist of Rhizoctonia solani. J Plant Pathol Microbiol 8:402.  https://doi.org/10.4172/2157-7471.1000402CrossRefGoogle Scholar
  2. Abdelrahman M, Abdel-Motaal F, El-Sayed M, Jogaiah S, Shigyo M, Ito SI, Tran LSP (2016) Dissection of Trichoderma longibrachiatum-induced defense in onion (Allium cepa L.) against Fusarium oxysporum f. sp. cepa by target metabolite profiling. Plant Sci 246:128–138PubMedGoogle Scholar
  3. Adams P, De-Leji FA, Lynch JM (2007) Trichoderma harzianum Rifai 1295-22 mediates growth promotion of crack willow (Salix fragilis) saplings in both clean and metal-contaminated soil. Microb Ecol 54(2):306–313PubMedGoogle Scholar
  4. Affokpon A, Coyne DL, Htay CC, Agbede RD, Lawouin L, Coosemans J (2011) Biocontrol potential of native Trichoderma isolates against root-knot nematodes in west African vegetable production systems. Soil Biol Biochem 43:600–608Google Scholar
  5. Afzal I, Basra SMA, Farooq M, Nawaz A (2006) Alleviation of salinity stress in spring wheat by hormonal priming with ABA, salicylic acid and ascorbic acid. Int J Agri Biol 8:23–28Google Scholar
  6. Agarwal S, Grover A (2006) Molecular biology, biotechnology and genomics of flooding-associated low O2 stress response in plants. Crit Rev Plant Sci 25:1–21.  https://doi.org/10.1080/07352680500365232CrossRefGoogle Scholar
  7. Ahmad JS, Baker R (1987) Rhizosphere competence of Trichoderma harzianum. Phytopathology 77(2):182–189Google Scholar
  8. Ahmad P, Hashem A, Abd-Allah EF, Alqarawi AA, John R, Egamberdieva D, Gucel S (2015) Role of Trichoderma harzianum in mitigating NaCl stress in Indian mustard (Brassica juncea L) through antioxidative defense system. Front Plant Sci 6:868.  https://doi.org/10.3389/fpls.2015.00868CrossRefPubMedPubMedCentralGoogle Scholar
  9. Alizadeh H, Behboudi K, Ahmadzadeh M, Javan-Nikkhah M, Zamioudis C, Pieterse CMJ, Bakker PAHM (2013) Induced systemic resistance in cucumber and Arabidopsis thaliana by the combination of Trichoderma harzianum Tr6 and Pseudomonas sp. Ps14. Biol Control 65:14–23Google Scholar
  10. Almeida FB, Cerqueira FM, Silva RN, Ulhoa CJ, Lima AL (2007) Mycoparasitism studies of Trichoderma harzianum strains against Rhizoctonia solani: evaluation of coiling and hydrolytic enzyme production. Biotechnol Lett 29:1189–1193.  https://doi.org/10.1007/s10529-007-9372-zCrossRefPubMedGoogle Scholar
  11. Alwhibi MS, Hashem A, Abd Allah EF, Egamberdieva D (2017) Increased resistance of drought by Trichoderma harzianum fungal treatment correlates with increased secondary metabolites and proline content. J Integr Agric 16(8):1751–1757.  https://doi.org/10.1016/S2095-3119(17)61695-2CrossRefGoogle Scholar
  12. Anam GB, Reddy MS, Ahn YH (2019) Characterization of Trichoderma asperellum RM-28 for its sodic/saline-alkali tolerance and plant growth promoting activities to alleviate toxicity of red mud. Sci Total Environ 662:462–469PubMedGoogle Scholar
  13. Anle H, Jianan S, Xinhua W, Liwen Z, Bo F, Jie C (2019) Reprogrammed endophytic microbial community in maize stalk induced by Trichoderma asperellum biocontrol agent against Fusarium diseases and mycotoxin accumulation. Fungal Biol 123:448–455Google Scholar
  14. Ansari MW, Trivedi DK, Sahoo RK, Gill SS, Tuteja N (2013) A critical review on fungi mediated plant responses with special emphasis to Piriformospora indica on improved production and protection of crops. Plant Physiol Biochem 70:403–410PubMedGoogle Scholar
  15. Babu AG, Shim J, Bang KS, Shea PJ, Oh BT (2014) Trichoderma virens PDR-28: a heavy metal-tolerant and plant growth-promoting fungus for remediation and bioenergy crop production on mine tailing soil. J Environ Manag 132:129–134.  https://doi.org/10.1016/j.jenvman.2013.10.009CrossRefGoogle Scholar
  16. Bae H, Sicher RC, Kim MS, Kim SH, Strem MD, Melnick RL, Bailey BA (2009) The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J Exp Bot 60(11):3279–3295.  https://doi.org/10.1093/jxb/erp165CrossRefPubMedPubMedCentralGoogle Scholar
  17. Bae H, Roberts DP, Lim HS, Strem MD, Park SC, Ryu CM, Melnick RL, Bailey BA (2011) Endophytic Trichoderma isolates from tropical environments delay disease onset and induce resistance against Phytophthora capsici in hot pepper using multiple mechanisms. Mol Plant-Microbe Interact 24:336–351PubMedGoogle Scholar
  18. Bae SJ, Mohanta TK, Chung JY, Ryu M, Park G, Shim S, Hong SB, Seo H, Bae DW, Bae I, Kim JJ (2016) Trichoderma metabolites as biological control agents against Phytophthora pathogens. Biol Control 92:128–138Google Scholar
  19. Bailey D, Lumsden R (1998) Direct effects of Trichoderma and Gliocladium on plant growth and resistance to pathogens. In: Harman GE, Kubicek CP (eds) Trichoderma and Gliocladium: enzymes, biological control and commercial applications, vol 2. Taylor & Francis, London, pp 185–204Google Scholar
  20. Battaglia D, Bossi S, Cascone P, Digilio MC, Duran Prieto J, Fanti P, Guerrieri E, Iodice L, Lingua G, Lorito M, Maffei ME, Massa N, Ruocco M, Sasso R, Trotta V (2013) Tomato below ground-above ground interactions: Trichoderma longibrachiatum affects the performance of Macrosiphum euphorbiae and its natural antagonists. Mol Plant-Microbe Interact 26:1249–1256Google Scholar
  21. Belanger RR, Dufour N, Caron J, Benhamou N (1995) Chronological events associated with the antagonistic properties of Trichoderma harzianum against Botrytis cinerea: indirect evidence for sequential role of antibiosis and parasitism. Biocontrol Sci Tech 5(1):41–54Google Scholar
  22. Benitez T, Rincon AM, Limón MC, Codon AC (2004) Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7:249–260Google Scholar
  23. Bernal-Vicente A, Pascual JA, Tittarelli F, Hernandezc JA, Diaz-Vivancos P (2015) Trichoderma harzianum T-78 supplementation of compost stimulates the antioxidant defence system in melon plants. J Sci Food Agric 95(11):2208–2214.  https://doi.org/10.1002/jsfa.6936CrossRefPubMedGoogle Scholar
  24. Bernat P, Nykiel-Szymańska J, Gajewska E, Różalska S, Stolarek P, Dackowa J, Słaba M (2018) Trichoderma harzianum diminished oxidative stress caused by 2,4- dichlorophenoxyacetic acid (2,4-D) in wheat, with insights from lipidomics. J Plant Physiol 229:158–163.  https://doi.org/10.1016/j.jplph.2018.07.010CrossRefPubMedGoogle Scholar
  25. Bhardwaj D, Ansari MW, Sahoo RK, Tuteja N (2014) Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microb Cell Factories 13(1):66Google Scholar
  26. Błaszczyk L, Siwulski M, Sobieralski K, Lisiecka J, Jedryczka M (2014) Trichoderma spp. – application and prospects for use in organic farming and industry. J Plant Prot Res 54(4):309–317.  https://doi.org/10.2478/jppr-2014-0047CrossRefGoogle Scholar
  27. Boyer JS (1982) Plant productivity and environment. Science 218:443–448Google Scholar
  28. Braun H, Woitsch L, Hetzer B, Geisen R, Zange B, Schmidt-Heydt M (2018) Trichoderma harzianum: inhibition of mycotoxin producing fungi and toxin biosynthesis. Int J Food Microbiol 280:10–16PubMedGoogle Scholar
  29. Brotman Y, Landau U, Cuadros-Inostroza A, Takayuki T, Fernie AR (2013) Trichoderma-plant root colonization: escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. PLoS Pathog 9(3):e1003221.  https://doi.org/10.1371/journal.ppat.1003221CrossRefPubMedPubMedCentralGoogle Scholar
  30. Brozová J (2004) Mycoparasitic fungi Trichoderma spp. in plant protection. A review. Plant Protect Sci 40:63–74Google Scholar
  31. Bunbury-Blanchette AL, Walker AK (2019) Trichoderma species show biocontrol potential in dual culture and greenhouse bioassays against Fusarium basal rot of onion. Biol Control 130:127–135Google Scholar
  32. Buragohain P, Sreedeep S, Lin P, Ni J, Garg A (2019) Influence of soil variability on single and competitive interaction of ammonium and potassium: experimental study on seven different soils. J Soils Sediments 19(1):186–197Google Scholar
  33. Caporale AG, Sommella A, Lorito M, Lombardi N, Azam SMGG, Pigna M, Ruocco M (2014) Trichoderma spp. alleviate phytotoxicity in lettuce plants (Lactuca sativa L.) irrigated with arsenic-contaminated water. J Plant Physiol 171:1378–1384PubMedGoogle Scholar
  34. Chaves MM, Oliveira MM (2004) Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. J Exp Bot 55:2365–2384.  https://doi.org/10.1093/jxb/erh269CrossRefGoogle Scholar
  35. Chaves M, Manuela P, Pereira JSM (2003) Understanding plant responses to drought-from genes to the whole plant. Funct Plant Biol 30:239–264Google Scholar
  36. Chen L, Yang X, Raza W, Li J, Liu Y, Qiu M, Zhang F, Shen Q (2011) Trichoderma harzianum SQR-T037 rapidly degrades allelochemicals in rhizospheres of continuously cropped cucumbers. Appl Microbiol Biotechnol 89(5):1653–1663Google Scholar
  37. Chen T, Yuan F, Song J, Wang B (2016) Nitric oxide participates in waterlogging tolerance through enhanced adventitious root formation in the euhalophyte Suaeda salsa. Funct Plant Biol 43(3):244–253PubMedGoogle Scholar
  38. Chet I, Harman GE, Baker R (1981) Trichoderma hamatum: its hyphal interactions with Rhizoctonia solani and Pythium spp. Microb Ecol 7(1):29–38Google Scholar
  39. Chowdappa P, Kumar SPM, Lakshmi MJ, Upreti KK (2013) Growth stimulation and induction of systemic resistance in tomato against early and late blight by Bacillus subtilis OTPB1 or Trichoderma harzianum OTPB3. Biol Control 65:109–117.  https://doi.org/10.1016/j.biocontrol.2012.11.009CrossRefGoogle Scholar
  40. Claydon N, Allan M, Hanson JR, Avent AG (1987) Antifungal alkyl pyrones of Trichoderma harzianum. Trans Br Mycol Soc 88(4):503–513Google Scholar
  41. Contreras-Cornejo HA, 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 149:1579–1592.  https://doi.org/10.1104/pp.108.130369CrossRefPubMedPubMedCentralGoogle Scholar
  42. Contreras-Cornejo HA, Macías-Rodríguez L, Alfaro-Cuevas R, Lopez-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(6):503–514.  https://doi.org/10.1094/MPMI-09-13-0265-RCrossRefPubMedGoogle Scholar
  43. Contreras-Cornejo HA, Macías-Rodríguez L, Vergara AG, López-Bucio J (2015) Trichoderma modulates stomatal aperture and leaf transpiration through an abscisic acid-dependent mechanism in Arabidopsis. J Plant Growth Regul 34(2):425–432Google Scholar
  44. 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):fiw036.  https://doi.org/10.1093/femsec/fiw036CrossRefGoogle Scholar
  45. Contreras-Cornejo HA, del-Val E, Macías-Rodríguez L, Alarcón A, González-Esquivel CE, Larsen J (2018) Trichoderma atroviride, a maize root associated fungus, increases the parasitism rate of the fall armyworm Spodoptera frugiperda by its natural enemy Campoletis sonorensis. Soil Biol Biochem 122:196–202Google Scholar
  46. Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163.  https://doi.org/10.1186/1471-2229-11-163CrossRefPubMedPubMedCentralGoogle Scholar
  47. De la Cruz-Quiroz R, Ascacio-Valdés JA, Rodríguez-Herrera R, Roussos S, Aguilar CN (2019) Phytopathogen biomass as inducer of antifungal compounds by Trichoderma asperellum under solid-state fermentation. In: Singh H, Keswani C, Reddy M, Sansinenea E, García-Estrada C (eds) Secondary metabolites of plant growth promoting rhizomicroorganisms. Springer, Singapore, pp 113–124Google Scholar
  48. De Meyer G, Bigirimana J, Elad Y, Hofte M (1998) Induced systemic resistance in Trichoderma harzianum T39 biocontrol of Botrytis cinerea. Eur J Plant Pathol 104:279–286Google Scholar
  49. Degenkolb T, Dieckmann R, Nielsen KF, Grafenhan T, Theis C, Zafari D, Chaverri P, Ismaiel A, Bruckner H, Von Dohren H, Thrane U, Petrini O, Samuels GJ (2008) The Trichoderma brevicompactum clade: a separate lineage with new species, new peptaibiotics, and mycotoxins. Mycol Prog 7:177–219.  https://doi.org/10.1007/s11557-008-0563-3CrossRefGoogle Scholar
  50. Dick RP (1992) A review: long-term effects of agricultural systems on soil biochemical and microbial parameters. Agric Ecosyst Environ 40(1-4):25–36Google Scholar
  51. Djonovic S, Pozo MJ, Dangott LJ, Howell CR, Kenerley CM (2006) Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defense responses and systemic resistance. Mol Plant-Microbe Interact 19:838–853PubMedGoogle Scholar
  52. Djonovic S, Vittone G, Mendoza-Herrera A, Kenerley CM (2007) Enhanced biocontrol activity of Trichoderma virens transformants constitutively coexpressing β-1, 3-and β-1, 6-glucanase genes. Mol Plant Pathol 8(4):469–480PubMedGoogle Scholar
  53. Doni F, Isahak A, Zain CRCM, Yusoff WMW (2014) Physiological and growth response of rice plants (Oryza sativa L.) to Trichoderma spp. inoculants. AMB Express 4(1):45PubMedPubMedCentralGoogle Scholar
  54. Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP (2011) Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9:749–759Google Scholar
  55. Ehrlich PR, Ehrlich AH (2016) Population, resources, and the faith-based economy: the situation in 2016. Biophys Econ Resour Qual 1:3.  https://doi.org/10.1007/s41247-016-0003-yCrossRefGoogle Scholar
  56. Eisendle M, Oberegger H, Buttinger R, Illmer P, Haas H (2004) Biosynthesis and uptake of siderophores is controlled by the PacC-mediated ambient-pH regulatory system in Aspergillus nidulans. Euk Cell 3:561–563Google Scholar
  57. Elamathi E, Malathi P, Viswanathan R, Ramesh Sundar A (2018) Expression analysis on mycoparasitism related genes during antagonism of Trichoderma with Colletotrichum falcatum causing red rot in sugarcane. J Plant Biochem Biot 27(3):351–361.  https://doi.org/10.1007/s13562-018-0444-zCrossRefGoogle Scholar
  58. Essah PA, Davenport R, Tester M (2003) Sodium influx and accumulation in Arabidopsis. Plant Physiol 133:307–318PubMedPubMedCentralGoogle Scholar
  59. Fridovich I (1986) Superoxide dismutases. Adv Enzymol Relat Areas Mol Biol 58(6):61–97PubMedGoogle Scholar
  60. Fu J, Liu Z, Li Z, Wang Y, Yang K (2017) Alleviation of the effects of saline-alkaline stress on maize seedlings by regulation of active oxygen metabolism by Trichoderma asperellum. PLoS One 12(6):e0179617PubMedPubMedCentralGoogle Scholar
  61. Fu J, Wang YF, Liu ZH, Li ZT, Yang KJ (2018) Trichoderma asperellum alleviates the effects of saline–alkaline stress on maize seedlings via the regulation of photosynthesis and nitrogen metabolism. Plant Growth Regul 85(3):363–374Google Scholar
  62. Gajera HP, Bambharolia RP, Patel SV, Khatrani TJ, Goalkiya BA (2012) Antagonism of Trichoderma spp. against Macrophomina phaseolina: evaluation of coiling and cell wall degrading enzymatic activities. J Plant Pathol Microb 3:149.  https://doi.org/10.4172/2157-7471.1000149CrossRefGoogle Scholar
  63. Gallo M, Esposito G, Ferracane R, Vinale F, Naviglio D (2013) Beneficial effects of Trichoderma genus microbes on qualitative parameters of Brassica rapa L. subsp. sylvestris L. Janch. Var. esculenta Hort. Eur Food Res Technol 236:1063–1071Google Scholar
  64. Ghisalberti EL, Sivasithamparam K (1991) Antifungal antibiotics produced by Trichoderma spp. Soil Biol Biochem 23(11):1011–1020Google Scholar
  65. Ghorbanpour A, Salimi A, Ghanbary MAT, Pirdashti H, Dehestani A (2018) The effect of Trichoderma harzianum in mitigating low temperature stress in tomato (Solanum lycopersicum L.) plants. Sci Hort 230:134–141Google Scholar
  66. Giuliani S, Sanguineti MC, Tuberosa R, Bellotti M, Salvi S, Landi P (2005) Root-ABA1 a major constitutive QTL affects maize root architecture and leaf ABA concentration at different water regimes. J Exp Bot 56:3061–3070Google Scholar
  67. Godfray HCJ, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818PubMedGoogle Scholar
  68. Grover M, Ali Sk Z, Sandhya V, Rasul A, Venkateswarlu B (2011) Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World J Microbiol Biotechnol 27:1231–1240.  https://doi.org/10.1007/s11274-010-0572-7CrossRefGoogle Scholar
  69. Guler NS, Pehlivan N, Karaoglu SA, Guzel S, Bozdeveci A (2016) Trichoderma atroviride ID20G inoculation ameliorates drought stress-induced damages by improving antioxidant defence in maize seedlings. Acta Physiol Plant 38(6):132Google Scholar
  70. Guzmán-Guzmán P, Porras-Troncoso MD, Olmedo-Monfil V, Herrera-Estrella A (2018) Trichoderma species: versatile plant symbionts. Phytopathology 109(1):6–16Google Scholar
  71. Halperin SJ, Gilroy S, Lynch JP (2003) Sodium chloride reduces growth and cytosolic calcium, but does not affect cytosolic pH, in root hairs of Arabidopsis thaliana L. J Exp Bot 54:1269–1280PubMedGoogle Scholar
  72. Harman GE (2011) Trichoderma—not just for biocontrol anymore. Phytoparasitica 39:103–108.  https://doi.org/10.1007/s12600-011-0151-yCrossRefGoogle Scholar
  73. Harman GE, Lorito M, Lynch JM (2004a) Uses of Trichoderma spp. to alleviate or remediate soil and water pollution. Adv Appl Microbiol 56:313–330PubMedGoogle Scholar
  74. Harman GE, Howell CR, Vitarbo A, Chet I, Lorito M (2004b) Trichoderma species –opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56Google Scholar
  75. Harman GE, Herrera-Estrella AH, Horwitz BA, Lorito M (2012) Trichoderma – from basic biology to biotechnology. Microbiology 158:1–2. (Special issue: 498)PubMedGoogle Scholar
  76. Hashem A, Abd_Allah EF, Alqarawi AA, Al Huqail AA, Egamberdieva D (2014) Alleviation of abiotic salt stress in Ochradenus baccatus (Del.) by Trichoderma hamatum (Bonord.) Bainier. J Plant Interact 9(1):857–868Google Scholar
  77. Hermosa MR, Keck E, Chamorro I, Rubio B, Sanz L, Vizcaino JA, Grondona I, Monte E (2004) Genetic diversity shown in Trichoderma biocontrol isolates. Mycol Res 108:897–906PubMedGoogle Scholar
  78. Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25.  https://doi.org/10.1099/mic.0.052274-0CrossRefGoogle Scholar
  79. Hermosa R, Rubio MB, Cardoza RE, Nicolas C, Monte E, Gutierrez S (2013) The contribution of Trichoderma to balancing the costs of plant growth and defense. Int Microbiol 16:69–80Google Scholar
  80. Hider RC, Kong X (2010) Chemistry and biology of siderophores. Nat Prod Rep 27(5):637–657Google Scholar
  81. Hirel B, Le Gouis J, Ney B, Gallais A (2007) The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J Exp Bot 58:2369–2387.  https://doi.org/10.1093/jxb/erm097CrossRefGoogle Scholar
  82. Howell CR (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87:4–10Google Scholar
  83. 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 Tech 3(4):435–441Google Scholar
  84. Hung R, Lee S, Bennett JW (2013) Arabidopsis thaliana as a model system for testing the effects of Trichoderma volatile organic compounds. Fungal Ecol 6:19–26Google Scholar
  85. Huot B, Yao J, Montgomery BL, He SY (2014) Growth–defense tradeoffs in plants: a balancing act to optimize fitness. Mol Plant 7:1267–1287PubMedPubMedCentralGoogle Scholar
  86. Hyakumachi M, Kubota M (2003) Fungi as plant growth promoter and disease suppressor. In: Arora DK (ed) Fungal biotechnology in agricultural, Food and environmental application. Marcel Dekker, New York, pp 101–110Google Scholar
  87. Jaspers P, Kangasjärvi J (2010) Reactive oxygen species in abiotic stress signaling. Physiol Plant 138:405–413Google Scholar
  88. Kashyap PL, Rai P, Srivastava AK, Kumar S (2017) Trichoderma for climate resilient agriculture. World J Microbiol Biotechnol 33(8):155.  https://doi.org/10.1007/s11274-017-2319-1CrossRefGoogle Scholar
  89. Katori T, Ikeda A, Iuchi S, Kobayashi M, Shinozaki K, Maehashi K, Sakata Y, Tanaka S, Taji T (2010) Dissecting the genetic control of natural variation in salt tolerance of Arabidopsis thaliana accessions. J Exp Bot 61:1125–1138PubMedPubMedCentralGoogle Scholar
  90. Keller NP, Turner G, Bennett JW (2005) Fungal secondary metabolism – from biochemistry to genomics. Nat Rev Microbiol 3:937–947Google Scholar
  91. Khomari S, Golshan-Doust S, Seyed-Sharifi R, Davari M (2018) Improvement of soybean seedling growth under salinity stress by biopriming of high-vigour seeds with salt-tolerant isolate of Trichoderma harzianum. New Zeal J Crop Hort 46(2):117–132Google Scholar
  92. Korolev N, Rav David D, Elad Y (2008) The role of phytohormones in basal resistance and Trichoderma-induced systemic resistance to Botrytis cinerea in Arabidopsis thaliana. BioControl 53:667–683.  https://doi.org/10.1007/s10526-007-9103-3CrossRefGoogle Scholar
  93. Kubicek CP, Mach RL, Peterbauer CK, Lorito M (2001) Trichoderma: from genes to biocontrol. J Plant Pathol 83:11–23Google Scholar
  94. Lee S, Hung R, Yap M, Bennett JW (2015) Age matters: the effects of volatile organic compounds emitted by Trichoderma atroviride on plant growth. Arch Microbiol 197(5):723–727.  https://doi.org/10.1007/s00203-015-1104-5CrossRefPubMedGoogle Scholar
  95. Li R-X, Cai F, Pang G, Shen Q-R, Li R, Chen W (2015) Solubilisation of phosphate and micronutrients by Trichoderma harzianum and its relationship with the promotion of tomato plant growth. PLoS One 10(6):e0130081.  https://doi.org/10.1371/journal.pone.0130081CrossRefPubMedPubMedCentralGoogle Scholar
  96. Li Y, Sun R, Yu J, Saravanakumar K, Chen J (2016) Antagonistic and biocontrol potential of Trichoderma asperellum ZJSX5003 against the maize stalk rot pathogen Fusarium graminearum. Indian J Microbiol 56(3):318–327.  https://doi.org/10.1007/s12088-016-0581-9CrossRefPubMedPubMedCentralGoogle Scholar
  97. Li X, Zhang X, Wang X, Yang X, Cui Z (2019) Bioaugmentation-assisted phytoremediation of lead and salinity co-contaminated soil by Suaeda salsa and Trichoderma asperellum. Chemosphere 224:716–725PubMedGoogle Scholar
  98. Linkies A, Muller K, Morris K, Tureckova V, Wenk M, Cadman CSC, Corbineau F, Strnad M, Lynn JR, Finch-Savage WE, Leubner Metzger G (2009) Ethylene interacts with abscisic acid to regulate endosperm rupture during germination: a comparative approach using Lepidium sativum and Arabidopsis thaliana. Plant Cell 21:3803–3822PubMedPubMedCentralGoogle Scholar
  99. Liu SY, Liao CK, Lo CT, Yang HH, Lin KC, Peng KC (2016) Chrysophanol is involved in the biofertilization and biocontrol activities of Trichoderma. Physiol Mol Plant Pathol 96:1–7Google Scholar
  100. Lopez-Mondejar R, Bernal-Vicente A, Ros M, Tittarelli F, Canali S, Intrigiolo F, Pascual JA (2010) Utilisation of citrus compost-based growing media amended with Trichoderma harzianum T-78 in Cucumis melo L. seedling production. Bioresour Technol 101:3718–3723PubMedGoogle Scholar
  101. Lorito M (2009) 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.xCrossRefPubMedGoogle Scholar
  102. Macías-Rodríguez L, Guzmán-Gómez A, García-Juárez P, Contreras-Cornejo HA (2018) Trichoderma atroviride promotes tomato development and alters the root exudation of carbohydrates, which stimulates fungal growth and the biocontrol of the phytopathogen Phytophthora cinnamomi in a tripartite interaction system. FEMS Microbiol Ecol 94(9):fiy137.  https://doi.org/10.1093/femsec/fiy137CrossRefGoogle Scholar
  103. Malinich EA, Wang K, Mukherjee PK, Kolomiets M, Kenerley CM (2019) Differential expression analysis of Trichoderma virens RNA reveals a dynamic transcriptome during colonization of Zea mays roots. BMC Genomics 20(1):280.  https://doi.org/10.1186/s12864-019-5651-zCrossRefPubMedPubMedCentralGoogle Scholar
  104. Marfori EC, Kajiyama S, Fukusaki E, Kobayashi A (2002) Trichosetin, a novel tetramic acid antibiotic produced in dual culture of Trichoderma harzianum and Catharanthus roseus callus. Z Naturforsch C 57(5-6):465–470PubMedGoogle Scholar
  105. Marra R, Ambrosino P, Carbone V, Vinale F, Woo SL, Ruocco M, Ciliento R, Lanzuise S, Ferraioli S, Soriente I, Gigante S, Turra D, Fogliano V, Scala F, Lorito M (2006) Study of the three-way interaction between Trichoderma atroviride, plant and fungal pathogens by using a proteomic approach. Curr Genet 50(5):307–321Google Scholar
  106. Martinez-Medina A, Fernandez I, Sanchez-Guzman MJ, Jung SC, Pascual JA, Pozo MJ (2013) Deciphering the hormonal signalling network behind the systemic resistance induced by Trichoderma harzianum in tomato. Front Plant Sci 4:206.  https://doi.org/10.3389/fpls.2013.00206CrossRefPubMedPubMedCentralGoogle Scholar
  107. Martínez-Medina A, Alguacil MDM, Pascual JA, Van Wees SC (2014) Phytohormone profiles induced by Trichoderma isolates correspond with their biocontrol and plant growth-promoting activity on melon plants. J Chem Ecol 40:804–815.  https://doi.org/10.1007/s10886-014-0478-1CrossRefGoogle Scholar
  108. Martínez-Medina A, Van Wees SC, Pieterse CMJ (2017) 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(11):2691–2705.  https://doi.org/10.1111/pce.13016CrossRefGoogle Scholar
  109. Mastouri F, Bjorkman T, Harman GE (2010) Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology 100:1213–1221Google Scholar
  110. Mastouri F, Bjorkman T, Harman GE (2012) Trichoderma harzianum enhances antioxidant defense of tomato seedlings and resistance to water deficit. Mol Plant Microbe Interact 25:1264–1271PubMedGoogle Scholar
  111. Mathews JR, Sivparsad BJ, Laing MD (2019) Greenhouse evaluation of Trichoderma harzianum for the control of Sclerotinia wilt (Sclerotinia sclerotiorum) of sunflower. S Afr J Plant Soil 36(1):69–72Google Scholar
  112. Mathys J, De Cremer K, Timmermans P, Van Kerckhove S, Lievens B, Vanhaecke M, Cammue BPA, De Coninck B (2012) Genome-wide characterization of ISR induced in Arabidopsis thaliana by Trichoderma hamatum T382 against Botrytis cinerea infection. Front Plant Sci 3:1–25Google Scholar
  113. Meena KK, Sorty AM, Bitla UM, Choudhary K, Gupta P, Pareek A, Singh DP, Prabha R, Sahu PK, Gupta VK, Singh HB, Krishanani KK, Minhas PS (2017) Abiotic stress responses and microbe-mediated mitigation in plants: the omics strategies. Front Plant Sci 8:172.  https://doi.org/10.3389/fpls.2017.00172CrossRefPubMedPubMedCentralGoogle Scholar
  114. Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19.  https://doi.org/10.1016/j.tplants.2005.11.002CrossRefPubMedGoogle Scholar
  115. Mohapatra S, Mittra B (2017) Alleviation of Fusarium oxysporum induced oxidative stress in wheat by Trichoderma viride. Arch Phytopathol Plant Protect 50(1–2):4–96.  https://doi.org/10.1080/03235408.2016.1263052CrossRefGoogle Scholar
  116. Mok DWS, Mok MC (2001) Cytokinin metabolism and action. Annu Rev Plant Physiol Plant Mol Biol 52:89–118Google Scholar
  117. Monteiro VN, do Nascimento Silva R, Steindorff AS, Costa FT, Noronha EF, Ricart CA, de Sousa MV, Vainstein MH, Ulhoa CJ (2010) New insights in Trichoderma harzianum antagonism of fungal plant pathogens by secreted protein analysis. Curr Microbiol 61:298–305.  https://doi.org/10.1007/s00284-010-9611-8CrossRefPubMedGoogle Scholar
  118. Montero-Barrientos M, Hermosa R, Cardoza RE, Gutierrez S, Nicola C, Monte E (2010) Transgenic expression of the Trichoderma harzianum hsp70 gene increases Arabidopsis resistance to heat and other abiotic stresses. J Plant Physiol 167:659–665PubMedGoogle Scholar
  119. Moran-Diez E, Hermosa R, Ambrosino P, Cardoza RE, Gutierrez S, Lorito M, Monte E (2009) The ThPG1 endopolygalacturonase is required for the Trichoderma harzianum–plant beneficial interaction. Mol Plant-Microbe Interact 22:1021–1031PubMedGoogle Scholar
  120. Mukherjee PK, Latha J, Hadar R, Horwitz BA (2003) TmkA, a mitogen-activated protein kinase of Trichoderma virens, is involved in biocontrol properties and repression of conidiation in the dark. Eukaryot Cell 2:446–455PubMedPubMedCentralGoogle Scholar
  121. Mukherjee PK, Horwitz BA, Charles MK (2012) Secondary metabolism in Trichoderma – a genomic perspective. Microbiology 158:35–45.  https://doi.org/10.1099/mic.0.053629-0CrossRefGoogle Scholar
  122. Mukherjee PK, Hurley JF, Taylor JT, Puckhaber L, Lehner S, Druzhinina I, Schumacher R, Kenerley CM (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(2):606–611Google Scholar
  123. Muvea AM, Meyhofer R, Subramanian S, Poehling HM, Ekesi S, Maniania NK (2014) Colonization of onion roots by endophytic fungi and their impacts on the biology of Thrips tabaci. PLoS One 9(9):e108242.  https://doi.org/10.1371/journal.pone.0108242CrossRefPubMedPubMedCentralGoogle Scholar
  124. Nanda AK, Andrio E, Marino D, Pauly N, Dunand C (2010) Reactive oxygen species during plant-microorganism early interactions. J Integr Plant Biol 52(2):195–204PubMedGoogle Scholar
  125. Naseby DC, Pascual JA, Lynch JM (2000) Effect of biocontrol strains of Trichoderma on plant growth, Pythium ultimum populations, soil microbial communities and soil enzyme activities. J Appl Microbiol 88(1):161–169Google Scholar
  126. Nawrocka J, Malolepsza U (2013) Diversity in plant systemic resistance induced by Trichoderma. Biol Control 67(2):149–156.  https://doi.org/10.1016/j.biocontrol.2013.07.005CrossRefGoogle Scholar
  127. Newbery F, Qi A, Fitt BDL (2016) Modelling impacts of climate change on arable crop diseases: progress, challenges and applications. Curr Opin Plant Biol 32:101–109PubMedGoogle Scholar
  128. Nguyen D, Rieu I, Mariani C, van Dam NM (2016) How plants handle multiple stresses: hormonal interactions underlying responses to abiotic stress and insect herbivory. Plant Mol Biol 91(6):727–740PubMedPubMedCentralGoogle Scholar
  129. Nielsen KF, Gräfenhan T, Zafari D, Thrane U (2005) Trichothecene production by Trichoderma brevicompactum. J Agric Food Chem 53:8190–8196Google Scholar
  130. Nieto-Jacobo MF, Steyaert JM, Salazar-Badillo FB, Nguyen DV, Rostas M, Braithwaite M, De Souza JT, Jimenez-Bremont JF, Ohkura M, Stewart A, Mendoza-Mendoza A (2017) Environmental growth conditions of Trichoderma spp. affects indole acetic acid derivatives, volatile organic compounds, and plant growth promotion. Front Plant Sci 8:102.  https://doi.org/10.3389/fpls.2017.00102CrossRefPubMedPubMedCentralGoogle Scholar
  131. Nogueira-Lopez G, Greenwood DR, Middleditch M, Winefield C, Eaton C, Steyaert JM, Mendoza-Mendoza A (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 9:409PubMedPubMedCentralGoogle Scholar
  132. Omero C, Inbar J, Rocha-Ramirez V, Herrera-Estrela A, Chet I, Horwitz BA (1999) G proteins activators and cAMP promote mycoparasitic behavior in Trichoderma harzianum. Mycol Res 103(12):1637–1642Google Scholar
  133. Omomowo IO, Fadiji AE, Omomowo OI (2018) Assessment of bio-efficacy of Glomus versiforme and Trichoderma harzianum in inhibiting powdery mildew disease and enhancing the growth of cowpea. Ann Agric Sci 63(1):9–17Google Scholar
  134. Oros G, Naar Z (2017) Mycofungicide: Trichoderma based preparation for foliar applications. Am J Plant Sci 8(2):113–125Google Scholar
  135. Ortiz-Castro R, Contreras-Cornejo HA, Macias-Rodriguez L, Lopez-Bucio J (2009) The role of microbial signals in plant growth and development. Plant Signal Behav 4(8):701–712.  https://doi.org/10.4161/psb.4.8.9047CrossRefPubMedPubMedCentralGoogle Scholar
  136. Ortuno N, Castillo A, Miranda C, Magnus MIC, Soto X (2017) The use of secondary metabolites extracted from Trichoderma for plant growth promotion in the Andean highlands. Renewable Agric Food Syst 32(4):366–375.  https://doi.org/10.1017/S1742170516000302CrossRefGoogle Scholar
  137. Palyzová A, Svobodová K, Sokolová L, Novák J, Novotný Č (2019) Metabolic profiling of Fusarium oxysporum f. sp. conglutinans race 2 in dual cultures with biocontrol agents Bacillus amyloliquefaciens, Pseudomonas aeruginosa, and Trichoderma harzianum. Folia Microbiol 64:779–787.  https://doi.org/10.1007/s12223-019-00690-7CrossRefGoogle Scholar
  138. Pandey V, Ansari MW, Tula S, Yadav S, Sahoo RK, Shukla N, Bains G, Badal S, Chandra S, Gaur AK, Kumar A, Shukla A, Kumar J, Tuteja N (2016) Dose-dependent response of Trichoderma harzianum in improving drought tolerance in rice genotypes. Planta 243:1251–1264.  https://doi.org/10.1007/s00425-016-2482-xCrossRefGoogle Scholar
  139. Pascale A, Vinale F, Manganiello G, Nigro M, Lanzuise S, Ruocco M, Marra R, Lombardi N, Woo SL, Lorito M (2017) Trichoderma and its secondary metabolites improve yield and quality of grapes. Crop Prot 92:176–181Google Scholar
  140. Pehlivan N, Yesilyurt AM, Durmus N, Karaglu SA (2017) Trichoderma lixii ID11D seed biopriming mitigates dose dependent salt toxicity in maize. Acta Physiol Plant 39:79.  https://doi.org/10.1007/s11738-017-2375-zCrossRefGoogle Scholar
  141. Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295Google Scholar
  142. Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5(5):308–316Google Scholar
  143. Qi W, Zhao L (2013) Study of the siderophore-producing Trichoderma asperellum Q1 on cucumber growth promotion under salt stress. J Basic Microbiol 53(4):355–364PubMedGoogle Scholar
  144. Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401Google Scholar
  145. Rawat L, Singh Y, Shukla N, Kumar J (2011) Alleviation of the adverse effects of salinity stress in wheat (Triticum aestivum L.) by seed biopriming with salinity tolerant isolates of Trichoderma harzianum. Plant Soil 347:387–400.  https://doi.org/10.1007/s11104-011-0858-zCrossRefGoogle Scholar
  146. Rawat L, Bisht TS, Kukreti A, Prasad M (2016) Bioprospecting drought tolerant Trichoderma harzianum isolates promote growth and delay the onset of drought responses in wheat (Triticum aestivum L.). Mol Soil Biol 7(4):1–15.  https://doi.org/10.5376/msb.2016.07.0004CrossRefGoogle Scholar
  147. Reino JL, Guerrero RF, Hernandez-Galan R, Collado IG (2008) Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochem Rev 7:89–123.  https://doi.org/10.1007/s11101-006-9032-2CrossRefGoogle Scholar
  148. Rockstrom J, Williams J, Daily G, Noble A, Matthewa N, Gordon L, Wetterstand H, DeClerck F, Shah M, Steduto P, De Fraiture C, Hatibu N, Unver O, Bird J, Sibanda L, Smith J (2017) Sustainable intensification of agriculture for human prosperity and global sustainability. Ambio 46(1):4–17PubMedGoogle Scholar
  149. Rubio MB, Quijada NM, Pérez E, Domínguez S, Monte E, Hermosa R (2014) Identifying beneficial qualities of Trichoderma parareesei for plants. Appl Environ Microbiol 80(6):1864–1873.  https://doi.org/10.1128/AEM.03375-13CrossRefPubMedPubMedCentralGoogle Scholar
  150. Rubio MB, de Medeiros HA, Morán-Diez ME, Castillo P, Hermosa R, Monte E (2019) A split-root method to study systemic and heritable traits induced by Trichoderma in tomato plants. In: Reinhardt D, Sharma AK (eds) Methods in rhizosphere biology research. Springer, Singapore, pp 151–166Google Scholar
  151. Saber WI, Ghoneem KM, Rashad YM, Al-Askar AA (2017) Trichoderma harzianum WKY1: an indole acetic acid producer for growth improvement and anthracnose disease control in sorghum. Biocontrol Sci Tech 27(5):654–676Google Scholar
  152. Sachdev S, Singh RP (2016a) Studies on trends in use of pesticides and fertilizers for tomato cultivation in the vicinity of Lucknow, India. Int J Sci Technol Soc 2(1-2):49–54.  https://doi.org/10.18091/ijsts.v2i1-2.7542CrossRefGoogle Scholar
  153. Sachdev S, Singh RP (2016b) Current challenges, constraints and future strategies for development of successful market for biopesticides. Clim Change Environ Sustain 4(2):129–136.  https://doi.org/10.5958/2320-642X.2016.00014.4CrossRefGoogle Scholar
  154. Sachdev S, Singh RP (2018a) Root colonization: imperative mechanism for efficient plant protection and growth. MOJ Eco Environ Sci 3(4):240–242Google Scholar
  155. Sachdev S, Singh RP (2018b) Isolation, characterisation and screening of native microbial isolates for biocontrol of fungal pathogens of tomato. Clim Change Environ Sustain 6(1):46–58Google Scholar
  156. Sachdev S, Singh A, Singh RP (2018) Optimization of culture conditions for mass production and bio-formulation of Trichoderma using response surface methodology. 3 Biotech 8(8):360PubMedPubMedCentralGoogle Scholar
  157. Samolski I, Rincon AM, Pinzon LM, Viterbo A, Monte E (2012) The qid74 gene from Trichoderma harzianum has a role in root architecture and plant biofertilization. Microbiology 158:129–138Google Scholar
  158. Saravanakumar K, Yu C, Dou K, Wang M, Li Y, Chen J (2016) Synergistic effect of Trichoderma-derived antifungal metabolites and cell wall degrading enzymes on enhanced biocontrol of Fusarium oxysporum f. sp. cucumerinum. Biol Control 94:37–46Google Scholar
  159. Saxena A, Raghuwanshi R, Singh HB (2014) Trichoderma species mediated differential tolerance against biotic stress of phytopathogens in Cicer arietinum L. J Basic Microbiol 54:1–12.  https://doi.org/10.1002/jobm.201400317CrossRefGoogle Scholar
  160. Schirmbock M, Lorito M, Wang YL, Hayes CK, ArisanAtac I, Scala F, Harman GE, Kubicek CP (1994) Parallel formation and synergism of hydrolytic enzymes and peptaibol antibiotics, molecular mechanisms involved in the antagonistic action of Trichoderma harzianum against phytopathogenic fungi. Appl Environ Microbiol 60(12):4364–4370PubMedPubMedCentralGoogle Scholar
  161. Segarra G, Casanova E, Bellido D, Odena MA, Oliveira E, Trillas I (2007) Proteome, salicylic acid, and jasmonic acid changes in cucumber plants inoculated with Trichoderma asperellum strain T34. Proteomics 7(21):3943–3952Google Scholar
  162. Segarra G, Van der Ent S, Trillas I, Pieterse CMJ (2009) MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biol 11:90–96.  https://doi.org/10.1111/j.1438-8677.2008.00162.xCrossRefGoogle Scholar
  163. Sharma PK, Gothalwal R (2017) Trichoderma: a potent fungus as biological control agent. In: Singh JS, Seneviratne G (eds) Agro-environmental sustainability: managing crop health, vol 1. Springer, Cham, pp 113–125Google Scholar
  164. Sharma A, Johri BN (2003) Growth promoting influence of siderophore-producing Pseudomonas strains GRP3A and PRS9 in maize (Zea mays L.) under iron limiting conditions. Microbiol Res 158(3):243–248PubMedGoogle Scholar
  165. Sharma R, Joshi A, Dhaker RC (2012) A brief review on mechanism of Trichoderma fungus use as biological control agents. Int J Innovovat Bio Sci 2(4):200–210Google Scholar
  166. Sharma KK, Singh US, Sharma P, Kumar A, Sharma L (2015) Seed treatments for sustainable agriculture-a review. J Appl Nat Sci 7(1):521–539Google Scholar
  167. 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(1):248–254.  https://doi.org/10.1590/S1517-83822014005000036CrossRefPubMedPubMedCentralGoogle Scholar
  168. Shiva V (2016) The violence of the green revolution: third world agriculture, ecology, and politics. University Press of Kentucky, Lexington, KYGoogle Scholar
  169. Shoresh M, Yedidia I, Chet I (2005) Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology 95(1):76–84.  https://doi.org/10.1094/PHYTO-95-0076CrossRefGoogle Scholar
  170. Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43Google Scholar
  171. Silva RN, Silva SP, Brandao RL, Ulhoa CJ (2004) Regulation of N-acetyl-b-D-glucosaminidase produced by Trichoderma harzianum: evidence that cAMP controls its expression. Res Microbiol 155:667–671PubMedGoogle Scholar
  172. Singh BN, Singh BR, Sarma BK, Singh HB (2009) Potential chemoprevention of N-nitrosodiethylamine-induced hepatocarcinogenesis by polyphenolics from Acacia nilotica bark. Chem Biol Interact 181(1):20–28PubMedGoogle Scholar
  173. Singh BN, Singh A, Singh SP, Singh HB (2011) Trichoderma harzianum mediated reprogramming of oxidative stress response in root apoplast of sunflower enhances defence against Rhizoctonia solani. Eur J Plant Pathol 131:121–134Google Scholar
  174. Singh A, Sarma BK, Upadhyay RS, Singh HB (2013) Compatible rhizosphere microbes mediated alleviation of biotic stress in chickpea through enhanced antioxidant and phenylpropanoid activities. Microbiol Res 168(1):33–40Google Scholar
  175. Singh JS, Abhilash PC, Gupta VK (2016) Agriculturally important microbes in sustainable food production. Trends Biotechnol 34:773–775.  https://doi.org/10.1016/j.tibtech.2016.06.002CrossRefGoogle Scholar
  176. Sivasithamparam K, Ghisalberti EL (1998) Secondary metabolism in Trichoderma and Gliocladium. In: Harman GE, Kubicek CP (eds) Trichoderma and Gliocladium: basic biology taxonomy and genetics, vol 1. Taylor & Francis, London, pp 139–191Google Scholar
  177. Sriram S, Manasa SB, Savitha MJ (2009) Potential use of elicitors from Trichoderma in induced systemic resistance for the management of Phytophthora capsici in red pepper. J Biol Control 23:449–456Google Scholar
  178. Srivastava P, Singh R, Tripathi S, Raghubanshi AS (2016) An urgent need for sustainable thinking in agriculture—an Indian scenario. Ecol Indic 67:611–622Google Scholar
  179. Studholme DJ, Harris B, Le Cocq K, Winsbury R, Perera V, Ryder L, Ward JL, Beale MH, Thornton CR, Grant M (2013) Investigating the beneficial traits of Trichoderma hamatum GD12 for sustainable agriculture—insights from genomics. Front Plant Sci 4:258.  https://doi.org/10.3389/fpls.2013.00258CrossRefPubMedPubMedCentralGoogle Scholar
  180. Tartoura KAH, Youssef SA (2011) Stimulation of ROS-scavenging systems in squash (Cucurbita pepo L.) plants by compost supplementation under normal and low temperature conditions. Sci Hort 130:862–868Google Scholar
  181. Tijerino A, Hermosa R, Cardoza RE, Moraga J, Malmierca MG, Aleu J, Collado IG, Monte E, Gutierrez S (2011a) Overexpression of the Trichoderma brevicompactum tri5 gene: effect on the expression of the trichodermin biosynthetic genes and on tomato seedlings. Toxins (Basel) 3(9):1220–1232.  https://doi.org/10.3390/toxins3091220CrossRefGoogle Scholar
  182. Tijerino A, Cardoza RE, Moraga J, Malmierca MG, Vicente F, Aleu J, Collado IG, Gutiérrez S, Monte E, Hermosa R (2011b) Overexpression of the trichodiene synthase gene tri5 increases trichodermin production and antimicrobial activity in Trichoderma brevicompactum. Fungal Genet Biol 48:285–296Google Scholar
  183. Tripathi P, Singh PC, Mishra A, Srivastava S, Chauhan R, Awasthi S, Mishra S, Dwivedi S, Tripathi P, Kalra A, Tripathi RD, Nautiyal CS (2017) Arsenic tolerant Trichoderma sp. reduces arsenic induced stress in chickpea (Cicer arietinum). Environ Pollut 223:137–145.  https://doi.org/10.1016/j.envpol.2016.12.073CrossRefGoogle Scholar
  184. Troian RF, Steindorff AS, Ramada MHS, Arruda W, Ulhoa CJ (2014) Mycoparasitism studies of Trichoderma harzianum against Sclerotinia sclerotiorum: evaluation of antagonism and expression of cell wall-degrading enzymes genes. Biotechnol Lett 36(10):2095–2101Google Scholar
  185. Turner TR, James EK, Poole PS (2013) The plant microbiome. Genome Biol 14(6):209PubMedPubMedCentralGoogle Scholar
  186. 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 151:792–808PubMedPubMedCentralGoogle Scholar
  187. Vargas JT, Rodriguez-Monroy M, Meyer ML, Montes-Belmont R, Sepulveda-Jimenez G (2017) Trichoderma asperellum ameliorates phytotoxic effects of copper in onion (Allium cepa L.). Environ Exp Bot 136:85–93.  https://doi.org/10.1016/j.envexpbot.2017.01.009CrossRefGoogle Scholar
  188. Verbruggen E, Kiers ET, Bakelaar PN, Röling WF, van der Heijden MG (2012) Provision of contrasting ecosystem services by soil communities from different agricultural fields. Plant Soil 350(1-2):43–55Google Scholar
  189. Vieira PM, Zeilinger S, Brandao RS, Vianna GR, Georg RC, Gruber S, Aragao FJL, Ulhoa CJ (2018) Overexpression of an aquaglyceroporin gene in the fungal biocontrol agent Trichoderma harzianum affects stress tolerance, pathogen antagonism and Phaseolus vulgaris development. Biol Control 126:185–191.  https://doi.org/10.1016/j.biocontrol.2018.08.012CrossRefGoogle Scholar
  190. Vinale F, Marra R, Scala F, Ghisalberti EL, Lorito M, Sivasithamparam K (2006) Major secondary metabolites produced by two commercial Trichoderma strains active against different phytopathogens. Lett Appl Microbiol 43:143–148Google Scholar
  191. Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Barbetti MJ, Li H, Woo SL, Lorito M (2008) A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiol Mol Plant Pathol 72:80–86Google Scholar
  192. Vinale F, Ghisalberti EL, Sivasithamparam K, Marra R, Ritieni A, Ferracane R, Woo S, Lorito M (2009a) Factors affecting the production of Trichoderma harzianum secondary metabolites during the interaction with different plant pathogens. Lett Appl Microbiol 48(6):705–711Google Scholar
  193. Vinale F, Flematti G, Sivasithamparam K, Lorito M, Marra R, Skelton BW, Ghisalberti EL (2009b) Harzianic acid, an antifungal and plant growth promoting metabolite from Trichoderma harzianum. J Nat Prod 72(11):2032–2035.  https://doi.org/10.1021/np900548pCrossRefGoogle Scholar
  194. Vinale F, Arjona GI, Nigro M, Mazzei P, Piccolo A, Ruocco M, Woo S, Rosa DR, Herrera CL, Lorito M (2012) Cerinolactone, a hydroxylactone derivative from Trichoderma cerinum. J Nat Prod 75:103–106PubMedGoogle Scholar
  195. Vinale F, Nigroa M, Sivasithamparam K, Flematti G, Ghisalberti EL, Ruocco M, Varlese R, Marra R, Lanzuise S, Eid A, Woo SL, Lorito M (2013) Harzianic acid: a novel siderophore from Trichoderma harzianum. FEMS Microbiol Lett 347(2):123–129.  https://doi.org/10.1111/1574-6968.12231CrossRefGoogle Scholar
  196. Vinale F, Sivasithamparam K, Ghisalberti EL, Woo SL, Nigro M, Marra R, Lombardi N, Pascale A, Ruocco M, Lanzuise S, Manganiello G, Lorito M (2014a) Trichoderma secondary metabolites active on plants and fungal pathogens. The Open Mycology Journal 8(Suppl-1, M5):127–139Google Scholar
  197. Vinale F, Manganiello G, Nigro M, Mazzei P, Piccolo A, Pascale A, Ruocco M, Marra R, Lombardi N, Lanzuise S, Varlese R, Cavallo P, Lorito M, Woo SL (2014b) A novel fungal metabolite with beneficial properties for agricultural applications. Molecules 19:9760–9772.  https://doi.org/10.3390/molecules19079760CrossRefPubMedPubMedCentralGoogle Scholar
  198. Vinale F, Strakowska J, Mazzei P, Piccolo A, Marra R, Lombardi N, Manganiello G, Pascale A, Woo SL, Lorito M (2016) Cremenolide, a new antifungal, 10-member lactone from Trichoderma cremeum with plant growth promotion activity. Nat Prod Res 30(22):2575–2581.  https://doi.org/10.1080/14786419.2015.1131985CrossRefPubMedGoogle Scholar
  199. Vinci G, Cozzolino V, Mazzei P, Monda H, Spaccini R, Piccolo A (2018) An alternative to mineral phosphorus fertilizers: the combined effects of Trichoderma harzianum and compost on Zea mays, as revealed by 1 H NMR and GC-MS metabolomics. PLoS One 13(12):e0209664.  https://doi.org/10.1371/journal.pone.0209664CrossRefPubMedPubMedCentralGoogle Scholar
  200. Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK, Kumar V, Verma R, Upadhyay RG, Pandey M, Sharma S (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci 8:161.  https://doi.org/10.3389/fpls.2017.00161CrossRefPubMedPubMedCentralGoogle Scholar
  201. Viterbo A, Montero M, Ramot O, Friesem D, Monte E, Llobell A, Chet I (2002) Expression regulation of the endochitinase chit36 from Trichoderma asperellum (T. harzianum T-203). Curr Genet 42:114–122PubMedGoogle Scholar
  202. Vitti A, Pellegrini E, Nali C, Lovelli S, Sofo A, Valerio M, Scopa A, Nuzzaci M (2016) Trichoderma harzianum T-22 induces systemic resistance in tomato infected by cucumber mosaic virus. Front Plant Sci 7:1520.  https://doi.org/10.3389/fpls.2016.01520CrossRefPubMedPubMedCentralGoogle Scholar
  203. Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14.  https://doi.org/10.1007/s00425-003-1105-5CrossRefGoogle Scholar
  204. Wang M, Hashimoto M, Hashidoko Y (2013) Repression of tropolone production and induction of a Burkholderia plantarii pseudo-biofilm by Carot-4-en-9,10-diol, a cell-to-cell signaling disrupter produced by Trichoderma virens. PLoS One 8(11):e78024.  https://doi.org/10.1371/journal.pone.0078024CrossRefPubMedPubMedCentralGoogle Scholar
  205. Wang X, Xu S, Wu S, Feng S, Bai Z, Zhuang G, Zhuang X (2018) Effect of Trichoderma viride biofertilizer on ammonia volatilization from an alkaline soil in northern China. J Environ Sci 66:199–207Google Scholar
  206. Wani SH, Kumar V, Shriram V, Sah SK (2016) Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J 4(3):162–176.  https://doi.org/10.1016/j.cj.2016.01.010CrossRefGoogle Scholar
  207. Woo SL, Ruocco M, Vinale F, Nigro M, Marra R, Lombardi N, Pascale A, Lanzuise S, Manganiello G, Lorito M (2014) Trichoderma-based products and their widespread use in agriculture. The Open Mycology Journal 8(1):71–126Google Scholar
  208. Wu CY, Chen CL, Lee YH, Cheng YC, Wu YC, Shu HY, Gotz F, Liu ST (2007) Nonribosomal synthesis of fengycin on an enzyme complex formed by fengycin synthetases. J Biol Chem 282:5608–5616.  https://doi.org/10.1074/jbc.M609726200CrossRefPubMedGoogle Scholar
  209. Wu Q, Ni M, Dou K, Tang J, Ren J, Yu C, Chen J (2018) Co-culture of Bacillus amyloliquefaciens ACCC11060 and Trichoderma asperellum GDFS1009 enhanced pathogen-inhibition and amino acid yield. Microb Cell Factories 17(1):155Google Scholar
  210. Yasmeen R, Siddiqui ZS (2018) Ameliorative effects of Trichoderma harzianum on monocot crops under hydroponic saline environment. Acta Physiol Plant 40(1):4Google Scholar
  211. Yedidia I, Benhamou N, Chet I (1999) Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl Environ Microbiol 65(3):1061–1070PubMedPubMedCentralGoogle Scholar
  212. Yesilyurt AM, Pehlivan N, Durmus N, Karaoglu SA (2018) Trichoderma citrinoviride: a potent biopriming agent for the alleviation of salt stress in maize. Hacettepe J Biol Chem 46(1):101–111Google Scholar
  213. Youssef SA, Kamel A, Tartoura KA, Abdelraouf GA (2016) Evaluation of Trichoderma harzianum and Serratia proteamaculans effect on disease suppression, stimulation of ROS-scavenging enzymes and improving tomato growth infected by Rhizoctonia solani. Biol Control 100:79–86Google Scholar
  214. Zeilinger S, Omann M (2007) Trichoderma biocontrol: signal transduction pathways involved in host sensing and mycoparasitism. Gene Regul Syst Bio 1:227–234PubMedPubMedCentralGoogle Scholar
  215. Zhang S, Xu B, Zhang J, Gan Y (2018) Identification of the antifungal activity of Trichoderma longibrachiatum T6 and assessment of bioactive substances in controlling phytopathogens. Pest Biochem Physiol 147:59–66Google Scholar
  216. Zikmundova M, Drandarov K, Bigler L, Hesse M, Werner C (2002) Biotransformation of 2-benzoxazolinone and 2-hydroxy-1, 4-benzoxazin-3-one by endophytic fungi isolated from Aphelandra tetragona. Appl Environ Microbiol 68(10):4863–4870PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2020

Authors and Affiliations

  • Swati Sachdev
    • 1
  • Rana Pratap Singh
    • 1
  1. 1.Department of Environmental Science, School for Environmental SciencesBabasaheb Bhimrao Ambedkar UniversityLucknowIndia

Personalised recommendations