Advertisement

Trichoderma pp 35-59 | Cite as

Could Trichoderma Be a Plant Pathogen? Successful Root Colonization

  • Jorge PovedaEmail author
  • Daniel Eugui
  • Patricia Abril-Urias
Chapter
  • 61 Downloads
Part of the Rhizosphere Biology book series (RHBIO)

Abstract

Root colonization by Trichoderma requires a complex molecular dialogue between fungus and plant. This colonization is limited to the outermost layers of the root and does not penetrate the plant vascular bundle. It is possible for a symbiotic relationship to be established in which Trichoderma improves plant growth and development through increasing systemic resistance against future possible attacks from pests and/or pathogens, increasing tolerance to abiotic stresses (i.e. salinity, drought, low temperatures), improving the capacity to absorb nutrients and actively stimulating plant growth. Various studies have shown that the ability to activate plant defences via salicylic acid (SA) is essential for the proper development of root colonization. Otherwise, Trichoderma would cross the thin line between symbiotic microorganism and opportunistic pathogen, reaching the root vascular bundle and causing the death of the plant tissues.

Keywords

Trichoderma Root colonization Salicylic acid Benefits Plant pathogen 

References

  1. Adams P, De-Leij FAAM, 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):306–313.  https://doi.org/10.1007/s00248-006-9203-0CrossRefPubMedGoogle Scholar
  2. Alfano G, Ivey MLL, Cakir C, Bos JIB, Miller SA, Madden LV, Hoitink HAJ (2007) Systemic modulation of gene expression in tomato by Trichoderma hamatum 382. Phytopathology 97(4):429–437.  https://doi.org/10.1094/phyto-97-4-0429CrossRefPubMedPubMedCentralGoogle Scholar
  3. Alonso-Ramírez A, Poveda J, Martín I, Hermosa R, Monte E, Nicolás C (2014) Salicylic acid prevents Trichoderma harzianum from entering the vascular system of roots. Mol Plant Pathol 15(8):823–831.  https://doi.org/10.1111/mpp.12141CrossRefPubMedPubMedCentralGoogle Scholar
  4. Altomare C, Norvell WA, Björkman T, Harman GE (1999) Solubilization of phosphates and micronutrients by the plant-growth-promoting and biocontrol fungus. Appl Environ Microbiol 65(7):2926–2933CrossRefGoogle Scholar
  5. Alvarez-Nordström S (2014) Endophytic growth of Clonostachys rosea in tomato and Arabidopsis. Dissertation, The Swedish University of Agricultural Sciences, Uppsala, Suecia (Sweden)Google Scholar
  6. Azarmi R, Hajieghrari B, Giglou A (2012) Effect of Trichoderma isolates on tomato seedling growth response and nutrient uptake. Afr J Biotechnol 10(31):5850–5855.  https://doi.org/10.5897/ajb10.1600CrossRefGoogle Scholar
  7. 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
  8. Baiyee B, Ito SI, Sunpapao A (2019) Trichoderma asperellum T1 mediated antifungal activity and induced defense response against leaf spot fungi in lettuce (Lactuca sativa L.). Physiol Mol Plant Pathol 106:96–101.  https://doi.org/10.1016/j.pmpp.2018.12.009CrossRefGoogle Scholar
  9. Banik A (2019) Plant endophytes: true symbiont or opportunistic pathogens? EC Microbiol 15:533–535Google Scholar
  10. Bisen K, Keswani C, Patel JS, Sarma BK, Singh HB (2016) Trichoderma spp.: efficient inducers of systemic resistance in plants. In: Chaudhary DK, Verma A (eds) Microbial-mediated induced systemic resistance in plants. Springer, Singapore, pp 185–195CrossRefGoogle Scholar
  11. 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(2):779–789.  https://doi.org/10.1104/pp.108.116293CrossRefPubMedPubMedCentralGoogle Scholar
  12. Brotman Y, Lisec J, Méret M, Chet I, Willmitzer L, Viterbo A (2012) Transcript and metabolite analysis of the Trichoderma-induced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana. Microbiology 158(1):139–146.  https://doi.org/10.1099/mic.0.052621-0CrossRefPubMedPubMedCentralGoogle Scholar
  13. Brotman Y, Landau U, Cuadros-Inostroza A, Takayuki T, Fernie AR, Chet I, Viterbo A, Willmitzer L (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
  14. 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(3):455–463.  https://doi.org/10.1111/j.1469-8137.1993.tb03836.xCrossRefGoogle Scholar
  15. Cardoza RE, McCormick SP, Malmierca MG, Olivera ER, Alexander NJ, Monte E, Gutiérrez S (2015) Effects of trichothecene production on the plant defense response and fungal physiology: overexpression of the Trichoderma arundinaceum tri4 gene in T. harzianum. Appl Environ Microbiol 81(18):6355–6366.  https://doi.org/10.1128/AEM.01626-15CrossRefPubMedPubMedCentralGoogle Scholar
  16. Carrero-Carrón I, Rubio MB, Niño-Sánchez J, Navas-Cortés JA, Jiménez-Díaz RM, Monte E, Hermosa R (2018) Interactions between Trichoderma harzianum and defoliating Verticillium dahliae in resistant and susceptible wild olive clones. Plant Pathol 67(8):1758–1767.  https://doi.org/10.1111/ppa.12879CrossRefGoogle Scholar
  17. Chacón MR, Rodríguez Galán O, Benítez Fernández CT, Sousa S, Rey M, Llobell González A, Delgado Jarana J (2007) Microscopic and transcriptome analyses of early colonization of tomato roots by Trichoderma harzianum. Int Microbiol 10(1):19–27.  https://doi.org/10.2436/20.1501.01.4CrossRefPubMedPubMedCentralGoogle Scholar
  18. 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(3):1579–1592.  https://doi.org/10.1104/pp.108.130369CrossRefPubMedPubMedCentralGoogle Scholar
  19. Contreras-Cornejo HA, Ortiz-Castro R, López-Bucio J, Mukherjee PK (2013) Promotion of plant growth and the induction of systemic defence by Trichoderma: physiology, genetics and gene expression. In: Mukherjee PK, Horwitz BA, Singh US, Mala M, Schmoll M (eds) Trichoderma: biology and applications. CABI, Wallingford, pp 173–194CrossRefGoogle Scholar
  20. Contreras-Cornejo HA, Macías-Rodríguez L, López-Bucio J (2014) Enhanced plant immunity using Trichoderma. In: Gupta VK (ed) Biotechnology and biology of Trichoderma. Elsevier, Oxford, pp 495–504CrossRefGoogle Scholar
  21. Contreras-Cornejo HA, Macías-Rodríguez L, del-Val E, Larsen J (2018) The root endophytic fungus Trichoderma atroviride induces foliar herbivory resistance in maize plants. Appl Soil Ecol 124:45–53.  https://doi.org/10.1016/j.apsoil.2017.10.004CrossRefGoogle Scholar
  22. Coppola M, Cascone P, Chiusano ML, Colantuono C, Lorito M, Pennacchio F, Rao R, Woo SL, Guerrieri E, Digilio MC (2017) Trichoderma harzianum enhances tomato indirect defense against aphids. Insect Sci 24(6):1025–1033.  https://doi.org/10.1111/1744-7917.12475CrossRefPubMedGoogle Scholar
  23. Coppola M, Cascone P, Di Lelio I, Woo SL, Lorito M, Rao R, Pennacchio F, Guerrieri E, Digilio MC (2019) Trichoderma atroviride P1 colonization of tomato plants enhances both direct and indirect defence barriers against insects. Front Physiol 10:813.  https://doi.org/10.3389/fphys.2019.00813CrossRefPubMedPubMedCentralGoogle Scholar
  24. Crutcher FK, Moran-Diez ME, Ding S, Liu J, Horwitz BA, Mukherjee PK, Kenerley CM (2015) A paralog of the proteinaceous elicitor SM1 is involved in colonization of maize roots by Trichoderma virens. Fungal Biol 119(6):476–486.  https://doi.org/10.1016/j.funbio.2015.01.004CrossRefPubMedPubMedCentralGoogle Scholar
  25. Djonović 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(3):875–889.  https://doi.org/10.1104/pp.107.103689CrossRefPubMedPubMedCentralGoogle Scholar
  26. Donoso EP, Bustamante RO, Caru M, Niemeyer HM (2008) Water deficit as a driver of the mutualistic relationship between the fungus Trichoderma harzianum and two wheat genotypes. Appl Environ Microbiol 74(5):1412–1417.  https://doi.org/10.1128/AEM.02013-07CrossRefPubMedPubMedCentralGoogle Scholar
  27. Elsharkawy MM, Shimizu M, Takahashi H, Ozaki K, Hyakumachi M (2013) Induction of systemic resistance against Cucumber mosaic virus in Arabidopsis thaliana by Trichoderma asperellum SKT-1. Plant Pathol J 29(2):193.  https://doi.org/10.5423/PPJ.SI.07.2012.01CrossRefPubMedPubMedCentralGoogle Scholar
  28. Fesel PH, Zuccaro A (2016) Dissecting endophytic lifestyle along the parasitism/mutualism continuum in Arabidopsis. Curr Opin Microbiol 32:103–112.  https://doi.org/10.1016/j.mib.2016.05.008CrossRefPubMedGoogle Scholar
  29. Filion M, St-Arnaud M, Fortin JA (1999) Direct interaction between the arbuscular mycorrhizal fungus Glomus intraradices and different rhizosphere microorganisms. New Phytol 141(3):525–533CrossRefGoogle Scholar
  30. Fiorini L, Guglielminetti L, Mariotti L, Curadi M, Picciarelli P, Scartazza A, Sarrocco S, Vannacci G (2016) Trichoderma harzianum T6776 modulates a complex metabolic network to stimulate tomato cv. Micro-Tom growth. Plant and Soil 400(1-2):351–366.  https://doi.org/10.1007/s11104-015-2736-6CrossRefGoogle Scholar
  31. Ghazanfar B, Cheng Z, Ahmad I, Khan AR, Hanqiang L, Haiyan D, Fang C (2015) Synergistic and individual effect of Glomus etunicatum root colonization and acetyl salicylic acid on root activity and architecture of tomato plants under moderate NaCl stress. Pak J Bot 47(6):2047–2054Google Scholar
  32. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227.  https://doi.org/10.1146/annurev.phyto.43.040204.135923CrossRefPubMedPubMedCentralGoogle Scholar
  33. Guzmán-Guzmán P, Porras-Troncoso MD, Olmedo-Monfil V, Herrera-Estrella A (2018) Trichoderma species: versatile plant symbionts. Phytopathology 109(1):6–16.  https://doi.org/10.1094/PHYTO-07-18-0218-RVWCrossRefPubMedPubMedCentralGoogle Scholar
  34. Harman GE (2000) Myths and dogmas of biocontrol changes in perceptions derived from research on Trichoderma harzianum T-22. Plant Dis 84(4):377–393.  https://doi.org/10.1094/PDIS.2000.84.4.377CrossRefPubMedGoogle Scholar
  35. Harman GE (2011) Trichoderma-not just for biocontrol anymore. Phytoparasitica 39(2):103–108.  https://doi.org/10.1007/s12600-011-0151-yCrossRefGoogle Scholar
  36. Harman GE, Lorito M, Chet I, Howell CR, Viterbo A (2004a) Trichoderma species- opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2(1):43–56.  https://doi.org/10.1038/nrmicro797CrossRefPubMedPubMedCentralGoogle Scholar
  37. Harman GE, Petzoldt R, Comis A, Chen J (2004b) Interactions between Trichoderma harzianum strain T22 and maize inbred line Mo17 and effects of these interactions on diseases caused by Pythium ultimum and Colletotrichum graminicola. Phytopathology 94(2):147–153.  https://doi.org/10.1094/phyto.2004.94.2.147CrossRefPubMedPubMedCentralGoogle Scholar
  38. Hermosa R, Viterbo A, Chet I, Monte EG (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158(1):17–25.  https://doi.org/10.1099/mic.0.052274-0CrossRefPubMedPubMedCentralGoogle Scholar
  39. Hermosa R, Rubio MB, Cardoza RE, Nicolás C, Monte E, Gutiérrez S (2013) The contribution of Trichoderma to balancing the costs of plant growth and defense. Int Microbiol 16(2):69–80.  https://doi.org/10.2436/20.1501.01.181CrossRefPubMedPubMedCentralGoogle Scholar
  40. Hoyos-Carvajal L, Orduz S, Bissett J (2009) Growth stimulation in bean (Phaseolus vulgaris L.) by Trichoderma. Biol Control 51(3):409–416.  https://doi.org/10.1016/j.biocontrol.2009.07.018CrossRefGoogle Scholar
  41. Jacobs S, Zechmann B, Molitor A, Trujillo M, Petutschnig E, Lipka V, Kogel KH, Schäfer P (2011) Broad-spectrum suppression of innate immunity is required for colonization of Arabidopsis roots by the fungus Piriformospora indica. Plant Physiol 156(2):726–740.  https://doi.org/10.1104/pp.111.176446CrossRefPubMedPubMedCentralGoogle Scholar
  42. de Jaeger N, Declerck S, de La Providencia IE (2010) Mycoparasitism of arbuscular mycorrhizal fungi: a pathway for the entry of saprotrophic fungi into roots. FEMS Microbiol Ecol 73(2):312–322.  https://doi.org/10.1111/j.1574-6941.2010.00903.xCrossRefPubMedGoogle Scholar
  43. Jogaiah S, Abdelrahman M, Tran LSP, Ito SI (2018) Different mechanisms of Trichoderma virens-mediated resistance in tomato against Fusarium wilt involve the jasmonic and salicylic acid pathways. Mol Plant Pathol 19(4):870–882.  https://doi.org/10.1111/mpp.12571CrossRefPubMedPubMedCentralGoogle Scholar
  44. Kleifeld O, Chet I (1992) Trichoderma harzianum-interaction with plants and effect on growth response. Plant and Soil 144:267–272.  https://doi.org/10.1007/BF00012884CrossRefGoogle Scholar
  45. Korolev N, David DR, Elad Y (2008) The role of phytohormones in basal resistance and Trichoderma-induced systemic resistance to Botrytis cinerea in Arabidopsis thaliana. Biol Control 53(4):667–683.  https://doi.org/10.1007/s10526-007-9103-3CrossRefGoogle Scholar
  46. Kubicek CP, Herrera-Estrella A, Seidl-Seiboth V, Martinez DA, Druzhinina IS, Thon M, Zeilinger S, Casas-Flores S, Horwitz BA, Mukherjee PK, Mukherjee M, László Kredics L, Luis D, Alcaraz LD, Aerts A, Zsuzsanna Antal Z, Atanasova L, Cervantes-Badillo MG, Challacombe J, Chertkov O, McCluskey K, Coulpier F, Deshpande N, von Döhren H, Ebbole DJ, Esquivel-Naranjo EU, Fekete E, Flipphi M, Glaser F, Gómez-Rodríguez EY, Gruber S, Han C, Henrissa B, Hermosa R, Miguel Hernández-Oñate M, Levente Karaffa L, Idit Kosti I, Le Crom S, Lindquist E, Lucas S, Lübeck M, Lübeck PS, Margeot A, Metz B, Misra M, Nevalainen H, Omann MN, Perrone G, Uresti-Rivera EE, Salamov A, Schmoll M, Seiboth B, Shapiro H, Sukno S, Tamayo-Ramos JA, Tisch D, Wiest A, Wilkinson HH, Michael Zhang M, Coutinho PM, Kenerley CM, Monte E, Baker SE, Grigoriev IV (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-r40CrossRefPubMedPubMedCentralGoogle Scholar
  47. Kubicek CP, Steindorff AS, Chenthamara K, Manganiello G, Henrissat B, Zhang J, Cai F, Kopchinskiy AG, Kubicek EM, Kuo A, Baroncelli R, Sarrocco S, Noronha EF, Vannacci G, Shen Q, Grigoriev IV, Druzhinina IS (2019) Evolution and comparative genomics of the most common Trichoderma species. BMC Genomics 20(1):485.  https://doi.org/10.1186/s12864-019-5680-7CrossRefPubMedPubMedCentralGoogle Scholar
  48. Lace B, Genre A, Woo S, Faccio A, Lorito M, Bonfante P (2015) Gate crashing arbuscular mycorrhizas: in vivo imaging shows the extensive colonization of both symbionts by Trichoderma atroviride. Environ Microbiol Rep 7(1):64–77.  https://doi.org/10.1111/1758-2229.12221CrossRefPubMedGoogle Scholar
  49. 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(4):1054–1063.  https://doi.org/10.1074/mcp.M114.046607CrossRefPubMedPubMedCentralGoogle Scholar
  50. de las Mercedes Dana M, Pintor-Toro JA, Cubero B (2006) Transgenic tobacco plants overexpressing chitinases of fungal origin show enhanced resistance to biotic and abiotic stress agents. Plant Physiol 142(2):722–730.  https://doi.org/10.1104/pp.106.086140CrossRefGoogle Scholar
  51. Lebeis SL, Paredes SH, Lundberg DS, Breakfield N, Gehring J, McDonald M, Malfatti S, Glavina del Rio T, Jones CD, Tringe SG, Dangl JL (2015) Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349(6250):860–864.  https://doi.org/10.1126/science.aaa8764CrossRefPubMedGoogle Scholar
  52. Li RX, Cai F, Pang G, Shen QR, 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):1–16.  https://doi.org/10.1371/journal.pone.0130081CrossRefGoogle Scholar
  53. Liang XR, Miao FP, Song YP, Guo ZY, Ji NY (2016) Trichocitrin, a new fusicoccane diterpene from the marine brown alga-endophytic fungus Trichoderma citrinoviride cf-27. Nat Prod Res 30(14):1605–1610.  https://doi.org/10.1080/14786419.2015.1126264CrossRefPubMedGoogle Scholar
  54. 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.2015.08.043CrossRefGoogle Scholar
  55. López-Ráez JA, Verhage A, Fernández I, García JM, Azcón-Aguilar C, Flors V, Pozo MJ (2010) Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot 61(10):2589–2601.  https://doi.org/10.1093/jxb/erq089CrossRefPubMedPubMedCentralGoogle Scholar
  56. Malmierca MG, McCormick SP, Cardoza RE, Monte E, Alexander NJ, Gutiérrez S (2015) Trichodiene production in a Trichoderma harzianum erg1-silenced strain provides evidence of the importance of the sterol biosynthetic pathway in inducing plant defense-related gene expression. Mol Plant Microbe Interact 28(11):1181–1197.  https://doi.org/10.1094/MPMI-06-15-0127-RCrossRefPubMedGoogle Scholar
  57. Marra R, Nicoletti R, Pagano E, DellaGreca M, Salvatore MM, Borrelli F, Lombardi N, Vinale F, Woo SL, Andolfi A (2019) Inhibitory effect of trichodermanone C, a sorbicillinoid produced by Trichoderma citrinoviride associated to the green alga Cladophora sp., on nitrite production in LPS-stimulated macrophages. Nat Prod Res 33:3389–3397.  https://doi.org/10.1080/14786419.2018.1479702CrossRefPubMedGoogle Scholar
  58. Martínez-Medina A, Roldán A, Albacete A, Pascual JA (2010) The interaction with arbuscular mycorrhizal fungi or Trichoderma harzianum alters the shoot hormonal profile in melon plants. Phytochemistry 72(2–3):223–229.  https://doi.org/10.1016/j.phytochem.2010.11.008CrossRefPubMedGoogle Scholar
  59. Martínez-Medina A, Fernández I, Sánchez-Guzmán 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
  60. Martínez-Medina A, Del Mar Alguacil M, Pascual JA, van Wees SCM (2014) Phytohormone profiles induced by Trichoderma isolates correspond with their biocontrol and plant growth-promoting activity on melon plants. J Chem Ecol 40(7):804–815.  https://doi.org/10.1007/s10886-014-0478-1CrossRefPubMedPubMedCentralGoogle Scholar
  61. Martínez-Medina A, Appels FV, van Wees SC (2017a) Impact of salicylic acid-and jasmonic acid-regulated defences on root colonization by Trichoderma harzianum T-78. Plant Signal Behav 12(8):e1345404.  https://doi.org/10.1080/15592324.2017.1345404CrossRefPubMedPubMedCentralGoogle Scholar
  62. Martínez-Medina A, van Wees SCM, Pieterse CMJ (2017b) 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.13016CrossRefPubMedGoogle Scholar
  63. Mastouri F, Björkman T, Harman GE (2010) Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology 100(11):1213–1221.  https://doi.org/10.1094/PHYTO-03-10-0091CrossRefPubMedPubMedCentralGoogle Scholar
  64. Mastouri F, Björkman T, Harman GE (2012) Trichoderma harzianum enhances antioxidant defense of tomato seedlings and resistance to water deficit. Mol Plant Microbe Interact 25(9):1264–1271.  https://doi.org/10.1094/mpmi-09-11-0240CrossRefPubMedGoogle Scholar
  65. Mathys J, De Cremer K, Timmermans P, van Kerkhove S, Lievens B, Vanhaecke M, Cammue BP, De Coninck B (2012) Genome-wide characterization of ISR induced in Arabidopsis thaliana by Trichoderma hamatum T382 against Botrytis cinerea infection. Front Plant Sci 3:108.  https://doi.org/10.3389/fpls.2012.00108CrossRefPubMedPubMedCentralGoogle Scholar
  66. de Medeiros HA, de Araújo Filho JV, De Freitas LG, Castillo P, Rubio MB, Hermosa R, Monte E (2017) Tomato progeny inherit resistance to the nematode Meloidogyne javanica linked to plant growth induced by the biocontrol fungus Trichoderma atroviride. Sci Rep 7:40216.  https://doi.org/10.1038/srep40216CrossRefPubMedPubMedCentralGoogle Scholar
  67. Medina MJH, Gagnon H, Piché Y, Ocampo JA, Garrido JMG, Vierheilig H (2003) Root colonization by arbuscular mycorrhizal fungi is affected by the salicylic acid content of the plant. Plant Sci 164(6):993–998.  https://doi.org/10.1016/S0168-9452(03)00083-9CrossRefGoogle Scholar
  68. Mendoza-Mendoza A, Zaid R, Lawry R, Hermosa R, Monte E, Horwitz BA, Mukherjee PK (2018) Molecular dialogues between Trichoderma and roots: role of the fungal secretome. Fungal Biol Rev 32(2):62–85.  https://doi.org/10.1016/j.fbr.2017.12.001CrossRefGoogle Scholar
  69. Mengel K, Kirkby EA (2001) Principles of plant nutrition. Springer, Dordrecht, p 635CrossRefGoogle Scholar
  70. de Meyer G, Bigiriman J, Elad Y, Höfte M (1998) Induced systemic resistance in Trichoderma harzianum T39 biocontrol of Botrytis cinerea. Eur J Plant Pathol 104(3):279–286.  https://doi.org/10.1023/A:1008628806616CrossRefGoogle Scholar
  71. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410.  https://doi.org/10.1016/S1360-1385(02)02312-9CrossRefPubMedPubMedCentralGoogle Scholar
  72. Montero-Barrientos M, Hermosa R, Cardoza RE, Gutiérrez S, Nicolás 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(8):659–665.  https://doi.org/10.1016/j.jplph.2009.11.012CrossRefPubMedGoogle Scholar
  73. Morán-Diez E, Hermosa R, Ambrosino P, Cardoza RE, Gutiérrez S, Lorito M, Monte E (2009) The ThPG1 endopolygalacturonase is required for the Trichoderma harzianum – plant beneficial interaction. Mol Plant Microbe Interact 22(8):1021–1031.  https://doi.org/10.1094/MPMI-22-8-1021CrossRefPubMedPubMedCentralGoogle Scholar
  74. Morán-Diez E, Rubio B, Domínguez S, Hermosa R, Monte E, Nicolás C (2012) Transcriptomic response of Arabidopsis thaliana after 24 h incubation with the biocontrol fungus Trichoderma harzianum. J Plant Physiol 169(6):614–620.  https://doi.org/10.1016/j.jplph.2011.12.016CrossRefPubMedGoogle Scholar
  75. Morán-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):8.  https://doi.org/10.1186/s12864CrossRefPubMedPubMedCentralGoogle Scholar
  76. Mukherjee M, Mukherjee PK, Horwitz BA, Zachow C, Berg G, Zeilinger S (2012) Trichoderma – plant–pathogen interactions: advances in genetics of biological control. Indian J Microbiol 52(4):522–529.  https://doi.org/10.1007/s12088-012-0308-5CrossRefPubMedPubMedCentralGoogle Scholar
  77. Nawrocka J, Małolepsza 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
  78. de Palma M, Salzano M, Villano C, Aversano R, Lorito M, Ruocco M, Docimo T, Piccinelli AL, D’Agostino N, Tucci M (2019) Transcriptome reprogramming, epigenetic modifications and alternative splicing orchestrate the tomato root response to the beneficial fungus Trichoderma harzianum. Hortic Res 6(1):5.  https://doi.org/10.1038/s41438-018-0079-1CrossRefPubMedPubMedCentralGoogle Scholar
  79. Pelagio-Flores R, Esparza-Reynoso S, Garnica-Vergara A, López-Bucio J, Herrera-Estrella A (2017) Trichoderma-induced acidification is an early trigger for changes in Arabidopsis root growth and determines fungal phytostimulation. Front Plant Sci 8:822.  https://doi.org/10.3389/fpls.2017.00822CrossRefPubMedPubMedCentralGoogle Scholar
  80. Peleg-Grossman S, Golani Y, Kaye Y, Melamed-Book N, Levine A (2009) NPR1 protein regulates pathogenic and symbiotic interactions between Rhizobium and legumes and non-legumes. PLoS One 4(12):e8399.  https://doi.org/10.1371/journal.pone.0008399CrossRefPubMedPubMedCentralGoogle Scholar
  81. Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10(4):393–398.  https://doi.org/10.1016/j.pbi.2007.05.004CrossRefPubMedPubMedCentralGoogle Scholar
  82. Rawat R, Tewari L (2011) Effect of abiotic stress on phosphate solubilization by biocontrol fungus Trichoderma sp. Curr Microbiol 62(5):1521–1526.  https://doi.org/10.1007/s00284-011-9888-2CrossRefPubMedGoogle Scholar
  83. Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62(10):3321–3338.  https://doi.org/10.1093/jxb/err031CrossRefPubMedGoogle Scholar
  84. 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
  85. 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(1):15–26.  https://doi.org/10.1007/s10658-011-9782-6CrossRefGoogle Scholar
  86. 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(1):129–138.  https://doi.org/10.1099/mic.0.053140-0CrossRefPubMedPubMedCentralGoogle Scholar
  87. Saravanakumar K, Fan L, Fu K, Yu C, Wang M, Xia H, Sun J, Yaqian L, Chen J (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/srep35543CrossRefPubMedPubMedCentralGoogle Scholar
  88. Searle LJ, Méric G, Porcelli I, Sheppard SK, Lucchini S (2015) Variation in siderophore biosynthetic gene distribution and production across environmental and faecal populations of Escherichia coli. PLoS One 10(3):1–14.  https://doi.org/10.1371/journal.pone.0117906CrossRefGoogle Scholar
  89. 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):3943–3952.  https://doi.org/10.1002/pmic.200700173CrossRefPubMedPubMedCentralGoogle Scholar
  90. Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plant 133(4):651–669.  https://doi.org/10.1111/j.1399-3054.2007.01008.xCrossRefGoogle Scholar
  91. Sharon E, Bar-Eyal M, Chet I, Herrera-Estrella A, Kleifeld O, Spiegel Y (2001) Biological control of the root-knot nematode Meloidogyne javanica by Trichoderma harzianum. Phytopathology 91(7):687–693.  https://doi.org/10.1094/PHYTO.2001.91.7.687CrossRefPubMedGoogle Scholar
  92. Shi ZZ, Fang ST, Miao FP, Yin XL, Ji NY (2018) 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.2018.08.027CrossRefPubMedGoogle Scholar
  93. Shoresh M, Harman GE (2008) The molecular basis of shoot responses of maize seedlings to Trichoderma harzianum T22 inoculation of the root: a proteomic approach. Plant Physiol 147(4):2147–2163.  https://doi.org/10.1104/pp.108.123810CrossRefPubMedPubMedCentralGoogle Scholar
  94. 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-95-0076CrossRefPubMedPubMedCentralGoogle Scholar
  95. 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-073009-114450CrossRefPubMedPubMedCentralGoogle Scholar
  96. Singh BN, Dwivedi P, Sarma BK, Singh GS, Singh HB (2018) Trichoderma asperellum T42 reprograms tobacco for enhanced nitrogen utilization efficiency and plant growth when fed with N nutrients. Front Plant Sci 9:163.  https://doi.org/10.3389/fpls.2018.00163CrossRefPubMedPubMedCentralGoogle Scholar
  97. Song YP, Liu XH, Shi ZZ, Miao FP, Fang ST, Ji NY (2018) Bisabolane, cyclonerane, and harziane derivatives from the marine-alga-endophytic fungus Trichoderma asperellum cf44-2. Phytochemistry 152:45–52.  https://doi.org/10.1016/j.phytochem.2018.04.017CrossRefPubMedGoogle Scholar
  98. van Spronsen PC, Tak T, Rood AM, van Brussel AA, Kijne JW, Boot KJ (2003) Salicylic acid inhibits indeterminate-type nodulation but not determinate-type nodulation. Mol Plant Microbe Interact 16(1):83–91.  https://doi.org/10.1094/MPMI.2003.16.1.83CrossRefPubMedGoogle Scholar
  99. 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(4):449–456Google Scholar
  100. Stacey G, McAlvin CB, Kim SY, Olivares J, Soto MJ (2006) Effects of endogenous salicylic acid on nodulation in the model legumes Lotus japonicus and Medicago truncatula. Plant Physiol 141(4):1473–1481.  https://doi.org/10.1104/pp.106.080986CrossRefPubMedPubMedCentralGoogle Scholar
  101. Su D, Ding L, He S (2018) Marine-derived Trichoderma species as a promising source of bioactive secondary metabolites. Mini Rev Med Chem 18(20):1702–1713.  https://doi.org/10.2174/1389557518666180727130826CrossRefPubMedGoogle Scholar
  102. Terry N, Zayed AM (1995) Physiology and biochemistry of leaves under iron deficiency. In Iron nutrition in soils and plants. In: Badìa J (ed) Iron nutrition in soils and plants. Kluwer Academic Publishers, Dordrecht, pp 283–294CrossRefGoogle Scholar
  103. Tucci M, Ruocco M, De Masi L, De Palma M, Lorito M (2011) The beneficial effect of Trichoderma spp. on tomato is modulated by the plant genotype. Mol Plant Pathol 12(4):341–354.  https://doi.org/10.1111/j.1364-3703.2010.00674.xCrossRefPubMedPubMedCentralGoogle Scholar
  104. 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):792–808.  https://doi.org/10.1104/pp.109.141291CrossRefPubMedPubMedCentralGoogle Scholar
  105. Velázquez-Robledo R, Contreras-Cornejo HA, Macías-Rodríguez L, Hernández-Morales A, Aguirre J, Casas-Flores S, López-Bucio J, Herrera-Estrella A (2011) Role of the 4-phosphopantetheinyl transferase of Trichoderma virens in secondary metabolism and induction of plant defense responses. Mol Plant Microbe Interact 24(12):1459–1471.  https://doi.org/10.1094/MPMI-02-11-0045CrossRefPubMedGoogle Scholar
  106. 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(1-2):157–174.  https://doi.org/10.1007/s11104-017-3445-0CrossRefGoogle Scholar
  107. Viterbo ADA, Chet I (2006) TasHyd1, a new hydrophobin gene from the biocontrol agent Trichoderma asperellum, is involved in plant root colonization. Mol Plant Pathol 7(4):249–258.  https://doi.org/10.1111/j.1364-3703.2006.00335.xCrossRefPubMedPubMedCentralGoogle Scholar
  108. 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(1):42–48.  https://doi.org/10.1111/j.1574-6968.2010.01910.xCrossRefPubMedPubMedCentralGoogle Scholar
  109. 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
  110. Vizcaíno JA, Cardoza RE, Hauser M, Hermosa R, Rey M, Llobell A, Becker JM, Gutiérrez S, Monte E (2006) ThPTR2, a di/tri-peptide transporter gene from Trichoderma harzianum. Fungal Genet Biol 43(4):234–246.  https://doi.org/10.1016/j.fgb.2005.12.003CrossRefPubMedPubMedCentralGoogle Scholar
  111. Welch RM, Norvell WA, Schaefer SC, Shaff JE, Kochian LV (1993) Induction of iron (III) and copper(II) reduction in pea (Pisum sativum L.) roots by Fe and Cu status: does the root-cell plasmalemma Fe(III)-chelate reductase perform a general role in regulating cation uptake? Planta 190(4):555–561.  https://doi.org/10.1007/BF00224795CrossRefGoogle Scholar
  112. Woo SL, Lorito M (2007) Exploiting the interactions between fungal antagonists, pathogens and the plant for biocontrol. In: Vurro M, Gressel J (eds) Novel biotechnologies for biocontrol agent enhancement and management. Springer, Dordrecht, pp 107–130CrossRefGoogle Scholar
  113. Yasmeen R, Siddiqui ZS (2018) Ameliorative effects of Trichoderma harzianum on monocot crops under hydroponic saline environment. Acta Physiol Plant 40(1):1–14.  https://doi.org/10.1007/s11738-017-2579-2CrossRefGoogle Scholar
  114. 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):1061–1070. 0099-2240/99/$04.0010CrossRefGoogle Scholar
  115. Yedidia I, Benhamou N, Kapulnik Y, Chet I (2000) Induction and accumulation of PR proteins activity during early stages of root colonization by the mycoparasite Trichoderma harzianum strain T-203. Plant Physiol Biochem 38(11):863–873.  https://doi.org/10.1016/S0981-9428(00)01198-0CrossRefGoogle Scholar
  116. Yedidia I, Srivastva AK, Kapulnik Y, Chet I (2001) Effect of Trichoderma harzianum on microelement concentrations and increased growth of cucumber plants. Plant and Soil 235(2):235–242.  https://doi.org/10.1023/A:1011990013955CrossRefGoogle Scholar
  117. Yoshioka Y, Ichikawa H, Naznin HA, Kogure A, Hyakumachi M (2011) Systemic resistance induced in Arabidopsis thaliana by Trichoderma asperellum SKT-1, a microbial pesticide of seedborne diseases of rice. Pest Manag Sci 68(1):60–66.  https://doi.org/10.1002/ps.2220CrossRefPubMedGoogle Scholar
  118. Yuan M, Huang Y, Ge W, Jia Z, Song S, Zhang L, Huang Y (2019) Involvement of jasmonic acid, ethylene and salicylic acid signaling pathways behind the systemic resistance induced by Trichoderma longibrachiatum H9 in cucumber. BMC Genomics 20(1):144.  https://doi.org/10.1186/s12864-019-5513-8CrossRefPubMedPubMedCentralGoogle Scholar
  119. Zamioudis C, Pieterse CM (2012) Modulation of host immunity by beneficial microbes. Mol Plant Microbe Interact 25(2):139–150.  https://doi.org/10.1094/MPMI-06-11-0179CrossRefPubMedPubMedCentralGoogle Scholar
  120. Zhang F, Meng X, Yang X, Ran W, Shen Q (2014) Quantification and role of organic acids in cucumber root exudates in Trichoderma harzianum T-E5 colonization. Plant Physiol Biochem 83:250–257.  https://doi.org/10.1016/j.plaphy.2014.08.011CrossRefPubMedGoogle Scholar
  121. Zhao L, Wang F, Zhang Y, Zhang J (2014) Involvement of Trichoderma asperellum strain T6 in regulating iron acquisition in plants. J Basic Microbiol 54(S1):115–124.  https://doi.org/10.1002/jobm.201400148CrossRefGoogle Scholar
  122. Zhu H, Zhang R, Chen W, Gu Z, Xie X, Zhao H, Yao Q (2015) The possible involvement of salicylic acid and hydrogen peroxide in the systemic promotion of phenolic biosynthesis in clover roots colonized by arbuscular mycorrhizal fungus. J Plant Physiol 178:27–34.  https://doi.org/10.1016/j.jplph.2015.01.016CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2020

Authors and Affiliations

  • Jorge Poveda
    • 1
    • 2
    Email author
  • Daniel Eugui
    • 1
    • 3
  • Patricia Abril-Urias
    • 1
    • 4
  1. 1.Spanish-Portuguese Institute for Agricultural Research (CIALE)University of SalamancaSalamancaSpain
  2. 2.Biological Mission of Galicia (CSIC)PontevedraSpain
  3. 3.Blue Agro BioscienceNoainSpain
  4. 4.Institute of Environmental Sciences of Castilla-La Mancha (ICAM)University of Castilla-La ManchaToledoSpain

Personalised recommendations