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Trichoderma pp 61-79 | Cite as

Harnessing the Perception of Trichoderma Signal Molecules in Rhizosphere to Improve Soil Health and Plant Health

  • Sevugapperumal NakkeeranEmail author
  • Suppaiah Rajamanickam
  • Murugavel Vanthana
  • Perumal Renukadevi
  • Malaiyandi Muthamilan
Chapter
  • 55 Downloads
Part of the Rhizosphere Biology book series (RHBIO)

Abstract

In the fungal kingdom, Trichoderma is the most exploited biocontrol agent. It is known for its ability to colonize plant root, suppress many plant pathogens, and act as inducer of systemic resistance in plant and is also involved in growth promotional activities. The knowledge on rhizosphere signalling between plant root–Trichoderma interaction is highly essential to trigger the immune response and to improve plant health. There is a bidirectional perception of signal molecules for the successful establishment of its association. The interaction of Trichoderma starts with contact to the root surface, followed by attachment, penetration, and colonization. The signal molecules from root exudates and secretomes of Trichoderma are essential for successful accomplishment of a symbiotic relationship. Among the complex composition of root exudates, sucrose plays a vital role in the attraction of Trichoderma to the plant root system. The hydrophobin and swollenins and cysteine-rich proteins secreted by Trichoderma plays a role in each step towards successful plant root interaction. This review enlightens our knowledge on root–Trichoderma interaction and its ability to overcome plant’s defense mechanism to prove itself as a “true friend” to the plant system and for improvement of soil and plant health.

Keywords

Trichoderma Signal molecules Rhizosphere specificity Hydrophobin Swollenins 

References

  1. Abdel-Lateif K, Bogusz D, Hocher V (2012) The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and Frankia bacteria. Plant Signal Behav 7(6):636–641PubMedPubMedCentralCrossRefGoogle Scholar
  2. Altomare C, Norvell WA, Bjorkman T, Harman GB (1999) Solubilization of phosphates and micronutrients by the plant growth- promoting and biocontrol fungus Trichoderma harzianum Rifai 1295-22. Appl Environ Microbiol 65:2926–2933PubMedPubMedCentralCrossRefGoogle Scholar
  3. 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 106:1049–1055PubMedPubMedCentralCrossRefGoogle Scholar
  4. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681PubMedCrossRefGoogle Scholar
  5. Baroncelli R, Matarese F, Moncini L, Vannacci G, Vergara M (2016) Two endopolygalacturonase genes in Trichoderma virens: in silico characterization and expression during interaction with plants. J Phytopathol 164:18–28CrossRefGoogle Scholar
  6. Brotman Y, Briff E, Viterbo A, Chet I (2008) Role of swollenin, an expansin-like protein from Trichoderma, in plant root colonization. Plant Physiol 147:779–789PubMedPubMedCentralCrossRefGoogle Scholar
  7. Carpenter MA, Ridgway HJ, Stringer AM, Hay AJ, Stewart A (2008) Characterization of a Trichoderma hamatum monooxygenase gene involved in antagonistic activity against fungal plant pathogens. Curr Genet 53:193–205PubMedCrossRefGoogle Scholar
  8. Chacon M, Rodriuez-Galan O, Benitez T, Sousa S, Rey M, Llobell A, Delgado-Jarana J (2007) Microscopic and transcriptome analysis of early colonization of tomato roots by Trichoderma harzianum. Int Microbiol 10:19–27PubMedGoogle Scholar
  9. Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803PubMedCrossRefGoogle Scholar
  10. Contreras CHA, 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 149:1579–1592CrossRefGoogle Scholar
  11. Contreras-Cornejo HA, Macias-Rodriguez LI, Alfaro-Cuevas R (2014) Trichoderma improves growth of Arabidopsis seedlings under salt stress through enhanced root development, osmolite production and Na+ elimination through root exudates. Mol Plant Microbe Interact 27:503–514PubMedCrossRefGoogle Scholar
  12. Dabire TG, Bonzi S, Somda I, Legreve A (2016) Evaluation of the potential of Trichoderma harzianum as a plant growth promoter and biocontrol agent against Fusarium damping-off in onion in Burkina Faso. Asian J Plant Pathol 10(4):49–60CrossRefGoogle Scholar
  13. De Lorenzo G, Brutus A, Savatin DV, Sicilia F, Cervone F (2011) Engineering plant resistance by constructing chimeric receptors that recognize damage-associated molecular patterns (DAMPs). FEBS Lett 585:1521–1528PubMedCrossRefGoogle Scholar
  14. De Oliveira AL, Gallo M, Pazzagli L, Benedetti CE, Cappugi G, Scala A, Pantera B, Spisni A, Pertinhez TA, Cicero DO (2011) The structure of the elicitor Cerato-platanin (CP), the first member of the CP fungal protein family, reveals a double ψβ-barrel fold and carbohydrate binding. J Biol Chem 286:17560–17568PubMedPubMedCentralCrossRefGoogle Scholar
  15. Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities. FEMS Microbiol Ecol 72:313–327CrossRefPubMedGoogle Scholar
  16. Di Cologna NDM, Gomez-Mendoza DP, Zanoelo FF, Giannesi GC, de Alencar Guimaraes NC, de Souza Moreira LR, Ferreira Filho EX, Ricart CAO (2018) Exploring Trichoderma and Aspergillus secretomes: proteomics approaches for the identification of enzymes of biotechnological interest. Enzyme Microb Technol 109:1–10PubMedCrossRefGoogle Scholar
  17. 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 19:838–853PubMedCrossRefGoogle Scholar
  18. Djonovic S, Vargas WA, Kolomiets MV, Horndeski M, Wiest A, Kenerley CM (2007) A proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol 145:875–889PubMedPubMedCentralCrossRefGoogle Scholar
  19. 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 16:749–759CrossRefGoogle Scholar
  20. Fiorentino N, Ventorino V, Woo SL, Pepe O, De Rosa A, Gioia L, Romano I, Lombardi N, Napolitano M, Colla G, Rouphael Y (2018) Trichoderma-based biostimulants modulate rhizosphere microbial populations and improve N uptake efficiency, yield, and nutritional quality of leafy vegetables. Front Plant Sci 9:743PubMedPubMedCentralCrossRefGoogle Scholar
  21. Garnica-Vergara A, Barrera-Ortiz S, Munoz-Parra E, Raya-Gonzalez J, Mendez-Bravo A, Macias-Rodriguez L, Ruiz-Herrera LF, Lopez-Bucio J (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 209:1496–1512PubMedCrossRefGoogle Scholar
  22. Hajieghrari B (2010) Effects of some Iranian Trichoderma isolates on maize seed germination and seedling vigor. Afr J Biotechnol 9(28):4342–4347Google Scholar
  23. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species-opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56PubMedCrossRefGoogle Scholar
  24. Hayat S, Faraz A, Faizan M (2017) Root exudates: composition and impact on plant–microbe interaction. In: Ahmad I, Husain FM (eds) Biofilms plant soil health. Wiley Publications, New York, NY, pp 179–193CrossRefGoogle Scholar
  25. Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25PubMedCrossRefGoogle Scholar
  26. Hermosa R, Rubio MB, Cardoza RE, Nicolas C, Monte E, Gutierrez S (2013) The contribution of Trichoderma to balancing the cost of plant growth and defense. Int Microbiol 16:69–80PubMedGoogle Scholar
  27. Kamilova F, Validov S, Azarova T, Mulders I, Lugtenberg B (2005) Enrichment for enhanced competitive root tip colonizers selects for a new class of biocontrol bacteria. Environ Microbiol 7:1809–1817PubMedCrossRefGoogle Scholar
  28. Kou Y, Tan YH, Ramanujam R, Naqvi NI (2017) Structure-function analyses of the Pth11 receptor reveal an important role for CFEM motif and redox regulation in rice blast. New Phytol 214:330–342PubMedCrossRefGoogle Scholar
  29. Lamdan NL, Shalaby S, Ziv T, Kenerley CM, Horwitz BA (2015) Secretome of Trichoderma interacting with maize roots: role in induced systemic resistance. Mol Cell Proteomics 14:1054–1063PubMedPubMedCentralCrossRefGoogle Scholar
  30. 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):e0130081PubMedPubMedCentralCrossRefGoogle Scholar
  31. Li WC, Huang CH, Chen CL, Chuang YC, Tung SY, Wang TF (2017) Trichoderma reesei complete genome sequence, repeat-induced point mutation, and partitioning of CAZyme gene clusters. Biotechnol Biofuels 10:170PubMedPubMedCentralCrossRefGoogle Scholar
  32. Lilliana HC, Andres C, Walter O, Sergio O (2015) The effect of various isolates of Trichoderma spp. on nutrient uptake in beans (Phaseolus vulgaris) in two soil types. Rev Colomb Cienc Hortic 9(2):268–278Google Scholar
  33. Luo Y, Zhang DD, Dong XW, Zhao PB, Chen LL, Song XY, Wang XJ, Chen XL, Shi M, Zhang YZ (2010) Antimicrobial peptaibols induce defense responses and systemic resistance in tobacco against Tobacco mosaic virus. FEMS Microbiol Lett 313:120–126PubMedCrossRefGoogle Scholar
  34. Mahato S, Bhuju S, Shrestha J (2018) Effect of Trichoderma viride as biofertilizer on growth and yield of wheat. Malaysian J Sustain Agric 2(2):01–05CrossRefGoogle Scholar
  35. Malmierca MG, Cardoza RE, Alexander NJ, McCormick SP, Collado IG, Hermosa R, Monte E, Gutierrez S (2013) Relevance of trichothecenes in fungal physiology: disruption of tri5 in Trichoderma arundinaceum. Fungal Genet Biol 53:22–33PubMedCrossRefGoogle Scholar
  36. Malmierca MG, McCormick SP, Cardoza RE, Alexander NJ, Monte E, Gutierrez S (2015) Production of trichodiene by Trichoderma harzianum alters the perception of this biocontrol strain by plants and antagonized fungi. Environ Microbiol 17:2628–2646PubMedCrossRefGoogle Scholar
  37. 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 50:307–321PubMedCrossRefGoogle Scholar
  38. Martinez C, Blanc F, Le Claire E, Besnard O, Nicole M, Baccou CJ (2001) Salicylic acid and ethylene pathways are differentially activated in melon cotyledons by active or heat-denatured cellulase from Trichoderma longibrachiatum. Plant Physiol 127:334–344PubMedPubMedCentralCrossRefGoogle Scholar
  39. Martinez-Medina A, Antonio Roldan A, Pascual JA (2011) Interaction between arbuscular mycorrhizal fungi and Trichoderma harzianum under conventional and low input fertilization field condition in melon crops: growth response and Fusarium wilt biocontrol. Appl Soil Ecol 47:98–10CrossRefGoogle Scholar
  40. Molla AH, Haque MM, Haque MA, Ilias GNM (2012) Trichoderma-enriched biofertilizer enhances production and nutritional quality of tomato (Lycopersicon esculentum Mill.) and minimizes NPK fertilizer use. Agric Res 1(3):265–272CrossRefGoogle Scholar
  41. 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 22:1021–1031PubMedCrossRefGoogle Scholar
  42. Moran-Diez ME, Trushina N, Lamdan NL, Rosenfelder L, Mukherjee PK, Kenerley CM, Horwitz BA (2015) Host-specific transcriptomic pattern of Trichoderma virens during interaction with maize or tomato roots. BMC Genomics 16(1):8PubMedPubMedCentralCrossRefGoogle Scholar
  43. Mukherjee PK, Buensanteai N, Moran-Diez ME, Druzhinina IS (2012) 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 158:155–165PubMedCrossRefGoogle Scholar
  44. Naseby DC, Pascual JA, Lynch JM (2000) Effect of biocontrol strains of Trichoderma on plant growth, Pythium ultimum populations, soil microbial communities and soil enzyme activities. J Appl Microbiol 88:161–169PubMedCrossRefGoogle Scholar
  45. Nasser L, Weissman Z, Pinsky M, Amartely H, Dvir H, Kornitzer D (2016) Structural basis of haem-iron acquisition by fungal pathogens. Nat Microbiol 1:16156PubMedCrossRefGoogle Scholar
  46. Nihorimbere V, Ongena M, Cawoy H, Brostaux Y, Kakana P, Jourdan E, Thonart P (2010) Beneficial effects of Bacillus subtilis on field-grown tomato in Burundi: reduction of local Fusarium disease and growth promotion. Afr J Microbiol Res 4(11):1135–1142Google Scholar
  47. Nosir WS (2016) Trichoderma harzianum as a growth promoter and bio-control agent against Fusarium oxysporum f. sp. tuberosi. Adv Crop Sci Technol 4(2):217CrossRefGoogle Scholar
  48. Parra EH, Alejo JC, Zapata JAR (2017) Trichoderma strains as growth promoters in Capsicum annuum and as biocontrol agents in Meloidogyne incognita. Chilean J Agric Res 77(4):318–324CrossRefGoogle Scholar
  49. Ramirez-Valdespino CA, Casas-Flores S, Olmedo-Monfil V (2019) Trichoderma as a model to study effector-like molecules. Front Microbiol 10:1030PubMedPubMedCentralCrossRefGoogle Scholar
  50. Reddy VS, Shlykov MA, Castillo R, Sun EI, Saier MH Jr (2012) The major facilitator superfamily (MFS) revisited. FEBS J 279(11):2022–2035PubMedPubMedCentralCrossRefGoogle Scholar
  51. Rippa S, Adenier H, Derbaly M, Beven L (2007) The Peptaibol Alamethicin induces an rRNA-cleavage-associated death in Arabidopsis thaliana. Chem Biodivers 4:1360–1373PubMedCrossRefGoogle Scholar
  52. Ron M, Avni A (2004) The receptor for the fungal elicitor ethylene inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16:1604–1615PubMedPubMedCentralCrossRefGoogle Scholar
  53. 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 32:1049–1055PubMedCrossRefGoogle Scholar
  54. Rubio MB, Hermosa R, Reino JL, Collado I, Monte E (2009) Thctf1 transcription factor of Trichoderma harzianum is involved in 6-pentyl 2H-pyran-2-one production and antifungal activity. Fungal Genet Biol 46:17–27PubMedCrossRefGoogle Scholar
  55. Rubio MB, Domínguez S, Monte E, Hermosa R (2012) Comparative study of Trichoderma gene expression in interactions with tomato plants using high-density oligonucleotide microarrays. Microbiology 158:119–128PubMedCrossRefGoogle Scholar
  56. Rubio MB, Quijada NM, Perez E, Dominguez S, Monte E, Hermosa R (2014) Identifying beneficial qualities of Trichoderma parareesei for plants. Appl Environ Microbiol 80(6):1864–1873PubMedPubMedCentralCrossRefGoogle Scholar
  57. Sabnam N, Roy Barman S (2017) WISH, a novel CFEM GPCR is indispensable for surface sensing, asexual and pathogenic differentiation in rice blast fungus. Fungal Genet Biol 105:37–51PubMedCrossRefGoogle Scholar
  58. Salas-Marina MA, Silva-Flores MA, Uresti-Rivera EE, Castro-Longoria E, Herrera-Estrella A, Casas-Flores S (2011) Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance through jasmonic acid/ethylene and salicylic acid pathways. Eur J Plant Pathol 131:15–26CrossRefGoogle Scholar
  59. Samolski I, de Luis A, Vizcaino JA, Monte E, Suarez MB (2009) Gene expression analysis of the biocontrol fungus Trichoderma harzianum in the presence of tomato plants, chitin, or glucose using a high-density oligonucleotide microarray. BMC Microbiol 9:217PubMedPubMedCentralCrossRefGoogle Scholar
  60. Samolski I, Rincon A, Pinzon LM, Viterbo A, Monte E (2012) The qid74 gene from Trichoderma harzianum has a role in root architecture and plant biofertilization. Microbiology 158:129–138PubMedCrossRefGoogle Scholar
  61. Saravanakumar K, Fan L, Fu K, Yu C, Wang M, Xia H, Sun J, Li Y, Chen J (2016) Cellulase from Trichoderma harzianum interacts with roots and triggers induced systemic resistance to foliar disease in maize. Sci Rep 6:35543PubMedPubMedCentralCrossRefGoogle Scholar
  62. Sarrocco S, Matarese F, Baroncelli R, Vannacci G, Seidl-Seiboth V, Kubicek CP, Vergara M (2017) The constitutive endopolygalacturonase TvPG2 regulates the induction of plant systemic resistance by Trichoderma virens. Phytopathology 107:537–544PubMedCrossRefGoogle Scholar
  63. Schuster A, Schmoll M (2010) Biology and biotechnology of Trichoderma. Appl Microbiol Biotechnol 87:787–799PubMedPubMedCentralCrossRefGoogle Scholar
  64. 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 7:3943–3952PubMedCrossRefGoogle Scholar
  65. Seidl V, Marchetti M, Schandl R, Kubicek CP, Allmaier G, Kubicek CP (2006) Epl1, the major secreted protein of Hypocrea atroviridis on glucose, is a member of a strongly conserved protein family comprising plant defense response elicitors. FEBS J 273:4346–4359PubMedCrossRefGoogle Scholar
  66. Sharma P, Patel AN, Saini MK, Deep S (2012) Field demonstration of Trichoderma harzianum as a plant growth promoter in wheat (Triticum aestivum L). J Agric Sci 4:8Google Scholar
  67. Shoresh M, Gal-On A, Leibman D, Chet I (2006) Characterization of a mitogen-activated protein kinase gene from cucumber required for Trichoderma-conferred plant resistance. Plant Physiol 142:1169–1179PubMedPubMedCentralCrossRefGoogle Scholar
  68. Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43PubMedCrossRefGoogle Scholar
  69. Stergiopoulos I, De Wit PJGM (2009) Fungal effector proteins. Annu Rev Phytopathol 47:233–263PubMedCrossRefGoogle Scholar
  70. Takanashi K, Shitan N, Yazaki K (2014) The multidrug and toxic compound extrusion (MATE) family in plants. Plant Biotechnol 31:417–430CrossRefGoogle Scholar
  71. Taniguchi N, Honke K, Fukuda M (eds) (2011) Handbook of glycosyltransferases and related genes. Springer Science & Business Media, New York, NYGoogle Scholar
  72. Tijerino A, Cardoza RE, Moraga J, Malmierca MG, Vicente F, Aleu J, Collado IG, Gutierrez S, Monte E, Hermosa R (2011) Overexpression of the trichodiene synthase gene tri5 increases trichodermin production and antimicrobial activity in Trichoderma brevicompactum. Fungal Genet Biol 48:285–296PubMedCrossRefGoogle Scholar
  73. Vargas WA, Mandawe JC, Kenerley CM (2009) Plant-derived sucrose is a key element in the symbiotic association between Trichoderma virens and maize plants. Plant Physiol 151(2):792–808PubMedPubMedCentralCrossRefGoogle Scholar
  74. Vasumathi S, Eraivan AAK, Nakkeeran S (2016) Exploring the diversity of Trichoderma spp. and the synergistic activity of delivery systems for the management of Fusarium wilt of cucumber under protected cultivation. J Mycol Plant Pathol 46(4):311Google Scholar
  75. Velmourougane K, Prasanna R, Singh S, Chawla G, Kumar A, Saxena AK (2017) Modulating rhizosphere colonisation, plant growth, soil nutrient availability and plant defense enzyme activity through Trichoderma viride-Azotobacter chroococcum biofilm inoculation in chickpea. Plant and Soil 421:157.  https://doi.org/10.1007/s11104-017-3445-0CrossRefGoogle Scholar
  76. Vinodkumar S, Indumathi T, Nakkeeran S (2017) Trichoderma asperellum (NVTA2) as a potential antagonist for the management of stem rot in carnation under protected cultivation. Biol Control 113:58–64CrossRefGoogle Scholar
  77. 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 7:249–258PubMedCrossRefGoogle Scholar
  78. Viterbo A, Harel M, Horwitz BA, Chet I, Mukherjee PK (2005) Trichoderma mitogen-activated protein kinase signaling is involved in induction of plant systemic resistance. Appl Environ Microbiol 71:6241–6246PubMedPubMedCentralCrossRefGoogle Scholar
  79. Viterbo A, Wiest A, Brotman Y, Chet I, Kenerley C (2007) The 18 mer peptaibols from Trichoderma virens elicit plant defense responses. Mol Plant Pathol 8:737–746PubMedCrossRefGoogle Scholar
  80. 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 305:42–48PubMedCrossRefGoogle Scholar
  81. Woo SL, Scala F, Ruocco M, Lorito M (2006) The molecular biology of the interactions between Trichoderma spp., phytopathogenic fungi, and plants. Phytopathology 96:181–185PubMedCrossRefGoogle Scholar
  82. Yoshioka Y, Ichikawa H, Naznin HA, Kogure A, Hyakumachi M (2012) Systemic resistance induced in Arabidopsis thaliana by Trichoderma asperellum SKT-1, a microbial pesticide of seedborne diseases of rice. Pest Manag Sci 68:60–66PubMedCrossRefGoogle Scholar
  83. Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant Microbe Interact 25:139–150PubMedCrossRefGoogle Scholar
  84. Zhang F, Yang X, Ran W, Shen Q (2014) Fusarium oxysporum induces the production of proteins and volatile organic compounds by Trichoderma harzianum T-E5. FEMS Microbiol Lett 359:116–123PubMedCrossRefGoogle Scholar
  85. Zhang F, Xu X, Huo Y, Xiao Y (2019) Trichoderma-inoculation and mowing synergistically altered soil available nutrients, rhizosphere chemical compounds and soil microbial community, potentially driving alfalfa growth. Front Microbiol 9:3241PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2020

Authors and Affiliations

  • Sevugapperumal Nakkeeran
    • 1
    Email author
  • Suppaiah Rajamanickam
    • 1
  • Murugavel Vanthana
    • 1
  • Perumal Renukadevi
    • 1
  • Malaiyandi Muthamilan
    • 1
  1. 1.Department of Plant PathologyTamil Nadu Agricultural UniversityCoimbatoreIndia

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