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Annual Review of Phytopathology

Volume 51, 2013

Research in the Genome Era

Abstract

species are widely used in agriculture and industry as biopesticides and sources of enzymes, respectively. These fungi reproduce asexually by production of conidia and chlamydospores and in wild habitats by ascospores. species are efficient mycoparasites and prolific producers of secondary metabolites, some of which have clinical importance. However, the ecological or biological significance of this metabolite diversity is sorely lagging behind the chemical significance. Many strains produce elicitors and induce resistance in plants through colonization of roots. Seven species have now been sequenced. Comparison of a primarily saprophytic species with two mycoparasitic species has provided striking contrasts and has established that mycoparasitism is an ancestral trait of this genus. Among the interesting outcomes of genome comparison is the discovery of a vast repertoire of secondary metabolism pathways and of numerous small cysteine-rich secreted proteins. Genomics has also facilitated investigation of sexual crossing in , suggesting the possibility of strain improvement through hybridization.

Keyword(s): biocontrol, fungal-plant interactions, morphogenesis, mycoparasitism, secondary metabolism
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2013-08-04
2024-04-19
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Literature Cited

  1. Atanasova L, Le Crom S, Gruber S, Coulpier F, Seidl-Seiboth V. 1.  et al. 2013. Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism. BMC Genomics. 14:121 [Google Scholar]
  2. Bae H, Sicher RC, Kim MS, Kim SH, Strem MD. 2.  et al. 2009. The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J. Exp. Bot. 60:3279–95 [Google Scholar]
  3. Baker SE, Perrone G, Richardson NM, Gallo A, Kubicek CP. 3.  2012. Phylogenomic analysis of polyketide synthase–encoding genes in Trichoderma. Microbiology 158:147–54 [Google Scholar]
  4. Bayram O, Krappmann S, Ni M, Bok JW, Helmstaedt K. 4.  et al. 2008. VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320:1504–6 [Google Scholar]
  5. Benitez T, Rincon AM, Limon MC, Codon AC. 5.  2004. Biocontrol mechanisms of Trichoderma strains. Int. Microbiol. 7:249–60 [Google Scholar]
  6. Berrocal-Tito G, Sametz-Baron L, Eichenberg K, Horwitz BA, Herrera-Estrella A. 6.  1999. Rapid blue light regulation of a Trichoderma harzianum photolyase gene. J. Biol. Chem. 274:14288–94 [Google Scholar]
  7. Bigirimana J, De Meyer G, Poppe J, Elad Y, Höfte M. 7.  1997. Induction of systemic resistance on bean (Phaseolus vulgaris) by Trichoderma harzianum. Med. Fac. Landbouww Univ. Gent 62:1001–7 [Google Scholar]
  8. Brotman Y, Briff E, Viterbo A, Chet I. 8.  2008. Role of swollenin, an expansin-like protein from Trichoderma, in plant root colonization. Plant Physiol. 147:779–89 [Google Scholar]
  9. Brotman Y, Lisec J, Meret M, Chet I, Willmitzer L, Viterbo A. 9.  2012. Transcript and metabolite analysis of the Trichoderma-induced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana. Microbiology 158:139–46 [Google Scholar]
  10. Brunner K, Omann M, Pucher ME, Delic M, Lehner SM. 10.  et al. 2008. Trichoderma G protein-coupled receptors: functional characterisation of a cAMP receptor-like protein from Trichoderma atroviride. Curr. Genet. 54:283–99 [Google Scholar]
  11. Buensanteai N, Mukherjee PK, Horwitz BA, Cheng C, Dangott LJ, Kenerley CM. 11.  2010. Expression and purification of biologically active Trichoderma virens proteinaceous elicitor Sm1 in Pichia pastoris. Protein Expr. Purif. 72:131–38 [Google Scholar]
  12. Cardoza RE, Malmierca MG, Hermosa MR, Alexander NJ, McCormick SP. 12.  et al. 2011. Identification of loci and functional characterization of trichothecene biosynthesis genes in filamentous fungi of the genus Trichoderma. Appl. Environ. Microbiol. 77:4867–77 [Google Scholar]
  13. Carpenter MA, Stewart A, Ridgway HJ. 13.  2005. Identification of novel Trichoderma hamatum genes expressed during mycoparasitism using subtractive hybridisation. FEMS Microbiol. Lett. 251:105–12 [Google Scholar]
  14. Carreras-Villasenor N, Sanchez-Arreguin JA, Herrera-Estrella AH. 14.  2012. Trichoderma: sensing the environment for survival and dispersal. Microbiology 158:3–16 [Google Scholar]
  15. Casas-Flores S, Rios-Momberg M, Bibbins M, Ponce-Noyola P, Herrera-Estrella A. 15.  2004. BLR-1 and BLR-2, key regulatory elements of photoconidiation and mycelial growth in Trichoderma atroviride. Microbiology 150:3561–69 [Google Scholar]
  16. Castellanos F, Schmoll M, Martinez P, Tisch D, Kubicek CP. 16.  et al. 2010. Crucial factors of the light perception machinery and their impact on growth and cellulase gene transcription in Trichoderma reesei. Fungal Genet. Biol. 47:468–76 [Google Scholar]
  17. Chang Y-C, Chang Y-C, Baker R, Kleifeld O, Chet I. 17.  1986. Increased growth of plants in the presence of the biological control agent Trichoderma harzianum. Plant Dis. 70:145–48 [Google Scholar]
  18. Chen CL, Kuo HC, Tung SY, Hsu PW, Wang CL. 18.  et al. 2012. Blue light acts as a double-edged sword in regulating sexual development of Hypocrea jecorina (Trichoderma reesei). PLoS ONE 7:e44969 [Google Scholar]
  19. Chen LL, Liu LJ, Shi M, Song XY, Zheng CY. 19.  et al. 2009. Characterization and gene cloning of a novel serine protease with nematicidal activity from Trichoderma pseudokoningii SMF2. FEMS Microbiol. Lett. 299:135–42 [Google Scholar]
  20. Chen XL, Yang J, Peng YL. 20.  2011. Large-scale insertional mutagenesis in Magnaporthe oryzae by Agrobacterium tumefaciens–mediated transformation. Methods Mol. Biol. 722:213–24 [Google Scholar]
  21. Chovanec P, Hudecova D, Varecka L. 21.  2001. Vegetative growth, aging- and light-induced conidiation of Trichoderma viride cultivated on different carbon sources. Folia Microbiol. (Praha) 46:417–22 [Google Scholar]
  22. Clutterbuck AJ. 22.  1969. A mutational analysis of conidial development in Aspergillus nidulans. Genetics 63:317–27 [Google Scholar]
  23. Collemare J, Pianfetti M, Houlle AE, Morin D, Camborde L. 23.  et al. 2008. Magnaporthe grisea avirulence gene ACE1 belongs to an infection-specific gene cluster involved in secondary metabolism. New Phytol. 179:196–208 [Google Scholar]
  24. Contreras-Cornejo HA, Macias-Rodriguez L, Beltran-Pena E, Herrera-Estrella A, Lopez-Bucio J. 24.  2011. Trichoderma-induced plant immunity likely involves both hormonal and camalexin dependent mechanisms in Arabidopsis thaliana and confers resistance against necrotrophic fungi Botrytis cinerea. Plant Signal. Behav. 6:1554–63 [Google Scholar]
  25. Contreras-Cornejo HA, Macias-Rodriguez L, Cortes-Penagos C, Lopez-Bucio J. 25.  2009. Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol. 149:1579–92 [Google Scholar]
  26. Cook R, Baker K. 26.  1983. The Nature and Practice of Biological Control of Plant Pathogens St Paul, MN: Am. Phytopathol. Soc.
  27. Cortes C, Gutierrez A, Olmedo V, Inbar J, Chet I, Herrera-Estrella A. 27.  1998. The expression of genes involved in parasitism by Trichoderma harzianum is triggered by a diffusible factor. Mol. Gen. Genet. 260:218–25 [Google Scholar]
  28. Crutcher FK, Parich A, Schuhmacher R, Mukherjee PK, Zeilinger S, Kenerley CM. 28.  2013. A putative terpene cyclase, vir4, is responsible for the biosynthesis of volatile terpene compounds in the biocontrol fungus Trichoderma virens. Fungal Genet. Biol. In press. http://dx.doi.org/10.1016/j.fgb.2013.05.003
  29. Deacon J. 29.  2006. Fungal Biology Oxford UK: Blackwell
  30. Degenkolb T, Karimi Aghcheh R, Dieckmann R, Neuhof T, Baker SE. 30.  et al. 2012. The production of multiple small peptaibol families by single 14-module peptide synthetases in Trichoderma/Hypocrea. Chem. Biodivers. 9:499–535 [Google Scholar]
  31. De Respinis S, Vogel G, Benagli C, Tonolla M, Petrini O, Samuels GJ. 31.  2010. MALDI-TOF MS of Trichoderma: a model system for the identification of microfungi. Mycol. Progress 9:79–100 [Google Scholar]
  32. Dixit P, Mukherjee PK, Ramachandran V, Eapen S. 32.  2011. Glutathione transferase from Trichoderma virens enhances cadmium tolerance without enhancing its accumulation in transgenic Nicotiana tabacum. PLoS ONE 6:e16360 [Google Scholar]
  33. Dixit P, Mukherjee PK, Sherkhane PD, Kale SP, Eapen S. 33.  2011. Enhanced tolerance and remediation of anthracene by transgenic tobacco plants expressing a fungal glutathione transferase gene. J. Hazard. Mater. 192:270–76 [Google Scholar]
  34. Djonovic S, Pozo MJ, Dangott LJ, Howell CR, Kenerley CM. 34.  2006. Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defense responses and systemic resistance. Mol. Plant-Microbe Interact. 19:838–53 [Google Scholar]
  35. Djonovic S, Vargas WA, Kolomiets MV, Horndeski M, Wiest A, Kenerley CM. 35.  2007. A proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol. 145:875–89 [Google Scholar]
  36. Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM. 36.  et al. 2011. Trichoderma: the genomics of opportunistic success. Nat. Rev. Microbiol. 9:749–59 [Google Scholar]
  37. Ellison CE, Hall C, Kowbel D, Welch J, Brem RB. 37.  et al. 2011. Population genomics and local adaptation in wild isolates of a model microbial eukaryote. Proc. Natl. Acad. Sci. USA 108:2831–36 [Google Scholar]
  38. Etxebeste O, Garzia A, Espeso EA, Ugalde U. 38.  2010. Aspergillus nidulans asexual development: making the most of cellular modules. Trends Microbiol. 18:569–76 [Google Scholar]
  39. Friedl MA, Kubicek CP, Druzhinina IS. 39.  2008. Carbon source dependence and photostimulation of conidiation in Hypocrea atroviridis. Appl. Environ. Microbiol. 74:245–50 [Google Scholar]
  40. Friedl MA, Schmoll M, Kubicek CP, Druzhinina IS. 40.  2008. Photostimulation of Hypocrea atroviridis growth occurs due to a cross-talk of carbon metabolism, blue light receptors and response to oxidative stress. Microbiology 154:1229–41 [Google Scholar]
  41. Geremia RA, Goldman GH, Jacobs D, Ardiles W, Vila SB. 41.  et al. 1993. Molecular characterization of the proteinase-encoding gene, prb1, related to mycoparasitism by Trichoderma harzianum. Mol. Microbiol. 8:603–13 [Google Scholar]
  42. Glare T, Caradus J, Gelernter W, Jackson T, Keyhani N. 42.  et al. 2012. Have biopesticides come of age?. Trends Biotechnol. 30:250–58 [Google Scholar]
  43. Gressel JB, Hartmann KM. 43.  1968. Morphogenesis in Trichoderma: action spectrum of photoinduced sporulation. Planta 79:271–74 [Google Scholar]
  44. Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M. 44.  et al. 2012. The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res. 40:D26–32 [Google Scholar]
  45. Gruber S, Kubicek CP, Seidl-Seiboth V. 45.  2011. Differential regulation of orthologous chitinase genes in mycoparasitic Trichoderma species. Appl. Environ. Microbiol. 77:7217–26 [Google Scholar]
  46. Gruber S, Seidl-Seiboth V. 46.  2012. Self versus non-self: fungal cell wall degradation in Trichoderma. Microbiology 158:26–34 [Google Scholar]
  47. Gruber S, Vaaje-Kolstad G, Matarese F, Lopez-Mondejar R, Kubicek CP, Seidl-Seiboth V. 47.  2011. Analysis of subgroup C of fungal chitinases containing chitin-binding and LysM modules in the mycoparasite Trichoderma atroviride. Glycobiology 21:122–33 [Google Scholar]
  48. Gutter Y. 48.  1957. Effect of light on sporulation of Trichoderma viride Pers. ex Fries. Bull. Res. Counc. Israel Sect. D Bot. 5:273–86 [Google Scholar]
  49. Harkki A, Uusitalo J, Bailey M, Penttilä M, Knowles J. 49.  1989. A novel fungal expression system: secretion of active calf chymosin from the filamentous fungus Trichoderma reesei. Nat. Biotechnol. 7:596–603 [Google Scholar]
  50. Harman GE. 50.  2000. Myths and dogmas of biocontrol. Changes in perceptions derived from research on Trichoderma harzianum T-22. Plant Dis. 84:377–93 [Google Scholar]
  51. Harman GE. 51.  2006. Overview of mechanisms and uses of Trichoderma spp. Phytopathology 96:190–94 [Google Scholar]
  52. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M. 52.  2004. Trichoderma species: opportunistic, avirulent plant symbionts. Nat. Rev. Microbiol. 2:43–56 [Google Scholar]
  53. Hermosa R, Viterbo A, Chet I, Monte E. 53.  2012. Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25 [Google Scholar]
  54. Hernandez-Oñate MA, Esquivel-Naranjo EU, Mendoza-Mendoza A, Stewart A, Herrera-Estrella AH. 54.  2012. An injury-response mechanism conserved across kingdoms determines entry of the fungus Trichoderma atroviride into development. Proc. Natl. Acad. Sci. USA 109:14918–23 [Google Scholar]
  55. Herrera-Estrella A, Chet I. 55.  2004. The biological control agent Trichoderma from fundamentals to applications. Handbook of Fungal Biotechnology D Arora 147–56 New York: Marcel Dekker Inc. [Google Scholar]
  56. Horwitz BA, Gressel J, Malkin S, Epel BL. 56.  1985. Modified cryptochrome in vivo absorption in dim photosporulation mutants of Trichoderma. Proc. Natl. Acad. Sci. USA 82:2736–40 [Google Scholar]
  57. Ihrmark K, Asmail N, Ubhayasekera W, Melin P, Stenlid J, Karlsson M. 57.  2010. Comparative molecular evolution of Trichoderma chitinases in response to mycoparasitic interactions. Evol. Bioinforma. Online 6:1–26 [Google Scholar]
  58. Inbar J, Chet I. 58.  1992. Biomimics of fungal cell-cell recognition by use of lectin-coated nylon fibers. J. Bacteriol. 174:1055–59 [Google Scholar]
  59. Inch S, Gilbert J. 59.  2011. Scanning electron microscopy observations of the interaction between Trichoderma harzianum and perithecia of Gibberella zeae. Mycologia 103:1–9 [Google Scholar]
  60. Jaklitsch WM. 60.  2009. European species of Hypocrea. Part I. The green-spored species. Stud. Mycol. 63:1–91 [Google Scholar]
  61. Jones JD, Dangl JL. 61.  2006. The plant immune system. Nature 444:323–29 [Google Scholar]
  62. Kale SD, Gu B, Capelluto DG, Dou D, Feldman E. 62.  et al. 2010. External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142:284–95 [Google Scholar]
  63. Karimi-Aghcheh R, Bok JW, Phatale PA, Smith KM, Baker SE. 63.  et al. 2013. Functional analyses of Trichoderma reesei LAE1 reveal conserved and contrasting roles of this regulator. G3 (Bethesda) 3:369–78 [Google Scholar]
  64. Klein D, Eveleigh DE. 64.  1998. Ecology of Trichoderma. Trichoderma and Gliocaldium 1 Basic Biology, Taxonomy and Genetics CP Kubicek, GE Harman 57–73 London: Taylor and Francis [Google Scholar]
  65. Komon-Zelazowska M, Neuhof T, Dieckmann R, von Dohren H, Herrera-Estrella A. 65.  et al. 2007. Formation of atroviridin by Hypocrea atroviridis is conidiation associated and positively regulated by blue light and the G protein GNA3. Eukaryot. Cell 6:2332–42 [Google Scholar]
  66. Kubicek CP, Baker S, Gamauf C, Kenerley CM, Druzhinina IS. 66.  2008. Purifying selection and birth-and-death evolution in the class II hydrophobin gene families of the ascomycete Trichoderma/Hypocrea. BMC Evol. Biol. 8:4 [Google Scholar]
  67. Kubicek CP, Herrera-Estrella A, Seidl-Seiboth V, Martinez DA, Druzhinina IS. 67.  et al. 2011. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol. 12:R40 [Google Scholar]
  68. Kubicek CP, Mikus M, Schuster A, Schmoll M, Seiboth B. 68.  2009. Metabolic engineering strategies for the improvement of cellulase production by Hypocrea jecorina. Biotechnol. Biofuels 2:19 [Google Scholar]
  69. Kubicek CP, Muhlbauer G, Klotz M, John E, Kubicek-Pranz E. 69.  1988. Properties of a conidial-bound cellulase enzyme system from Trichoderma reesei. Microbiol. Mol. Biol. Rev. 134:1215–22 [Google Scholar]
  70. Kuhls K, Lieckfeldt E, Samuels GJ, Kovacs W, Meyer W. 70.  et al. 1996. Molecular evidence that the asexual industrial fungus Trichoderma reesei is a clonal derivative of the ascomycete Hypocrea jecorina. Proc. Natl. Acad. Sci. USA 93:7755–60 [Google Scholar]
  71. Kumagai T, Oda Y. 71.  1969. An action spectrum for photoinduced sporulation in fungus Trichoderma viride. Plant Cell Physiol. 10:387–92 [Google Scholar]
  72. Kumar A, Scher K, Mukherjee M, Pardovitz-Kedmi E, Sible GV. 72.  et al. 2010. Overlapping and distinct functions of two Trichoderma virens MAP kinases in cell-wall integrity, antagonistic properties and repression of conidiation. Biochem. Biophys. Res. Commun. 398:765–70 [Google Scholar]
  73. Le Crom S, Schackwitz W, Pennacchio L, Magnuson JK, Culley DE. 73.  et al. 2009. Tracking the roots of cellulase hyperproduction by the fungus Trichoderma reesei using massively parallel DNA sequencing. Proc. Natl. Acad. Sci. USA 106:16151–56 [Google Scholar]
  74. Lehner SM, Atanasova L, Neumann NK, Krska R, Lemmens M. 74.  et al. 2013. Isotope-assisted screening for iron-containing metabolites reveals high diversity among known and unknown siderophores produced by Trichoderma spp. Appl. Environ. Microbiol. 79:18–31 [Google Scholar]
  75. Lim FY, Sanchez JF, Wang CC, Keller NP. 75.  2012. Toward awakening cryptic secondary metabolite gene clusters in filamentous fungi. Methods Enzymol. 517:303–24 [Google Scholar]
  76. Liu Y, He Q, Cheng P. 76.  2003. Photoreception in Neurospora: a tale of two white collar proteins. Cell. Mol. Life Sci. 60:2131–38 [Google Scholar]
  77. Lorito M, Woo SL, Garcia I, Colucci G, Harman GE. 77.  et al. 1998. Genes from mycoparasitic fungi as a source for improving plant resistance to fungal pathogens. Proc. Natl. Acad. Sci. USA 95:7860–65 [Google Scholar]
  78. Lorito M, Woo SL, Harman GE, Monte E. 78.  2010. Translational research on Trichoderma: from ‘omics to the field. Annu. Rev. Phytopathol. 48:395–417 [Google Scholar]
  79. Malmierca MG, Cardoza RE, Alexander NJ, McCormick SP, Hermosa R. 79.  et al. 2012. Involvement of Trichoderma trichothecenes in the biocontrol activity and induction of plant defense–related genes. Appl. Environ. Microbiol. 78:4856–68 [Google Scholar]
  80. Martinez D, Berka RM, Henrissat B, Saloheimo M, Arvas M. 80.  et al. 2008. Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat. Biotechnol. 26:553–60 [Google Scholar]
  81. Mastouri F, Bjorkman T, Harman GE. 81.  2012. Trichoderma harzianum enhances antioxidant defense of tomato seedlings and resistance to water deficit. Mol. Plant-Microbe Interact. 25:1264–71 [Google Scholar]
  82. Mathys J, De Cremer K, Timmermans P, Van Kerckhove S, Lievens B. 82.  et al. 2012. Genome-wide characterization of ISR induced in Arabidopsis thaliana by Trichoderma hamatum T382 against Botrytis cinerea infection. Front. Plant Sci. 3:108 [Google Scholar]
  83. Mendoza-Mendoza A, Pozo MJ, Grzegorski D, Martinez P, Garcia JM. 83.  et al. 2003. Enhanced biocontrol activity of Trichoderma through inactivation of a mitogen-activated protein kinase. Proc. Natl. Acad. Sci. USA 100:15965–70 [Google Scholar]
  84. Metz B, Seidl-Seiboth V, Haarmann T, Kopchinskiy A, Lorenz P. 84.  et al. 2011. Expression of biomass-degrading enzymes is a major event during conidium development in Trichoderma reesei. Eukaryot. Cell 10:1527–35 [Google Scholar]
  85. Mikus M, Hatvani L, Neuhof T, Komon-Zelazowska M, Dieckmann R. 85.  et al. 2009. Differential regulation and posttranslational processing of the class II hydrophobin genes from the biocontrol fungus Hypocrea atroviridis. Appl. Environ. Microbiol. 75:3222–29 [Google Scholar]
  86. Montenecourt B, Eveleigh D. 86.  1979. Selective screening methods for the isolation of high yielding cellulase mutants of Trichoderma reesei. Adv. Chem. Ser. 181:289–301 [Google Scholar]
  87. Moran-Diez E, Hermosa R, Ambrosino P, Cardoza RE, Gutierrez S. 87.  et al. 2009. The ThPG1 endopolygalacturonase is required for the Trichoderma harzianum–plant beneficial interaction. Mol. Plant-Microbe Interact. 22:1021–31 [Google Scholar]
  88. Moran-Diez E, Rubio B, Dominguez S, Hermosa R, Monte E, Nicolas C. 88.  2012. Transcriptomic response of Arabidopsis thaliana after 24 h incubation with the biocontrol fungus Trichoderma harzianum. J. Plant Physiol. 169:614–20 [Google Scholar]
  89. Mukherjee M, Horwitz BA, Sherkhane PD, Hadar R, Mukherjee PK. 89.  2006. A secondary metabolite biosynthesis cluster in Trichoderma virens: evidence from analysis of genes underexpressed in a mutant defective in morphogenesis and antibiotic production. Curr. Genet. 50:193–202 [Google Scholar]
  90. Mukherjee M, Mukherjee PK, Horwitz BA, Zachow C, Berg G, Zeilinger S. 90.  2012. Trichoderma-plant-pathogen interactions: advances in genetics of biological control. Indian J. Microbiol. 52:522–29 [Google Scholar]
  91. Mukherjee PK, Buensanteai N, Moran-Diez ME, Druzhinina IS, Kenerley CM. 91.  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 158:155–65 [Google Scholar]
  92. Mukherjee PK, Horwitz BA, Kenerley CM. 92.  2012. Secondary metabolism in Trichoderma: a genomic perspective. Microbiology 158:35–45 [Google Scholar]
  93. Mukherjee PK, Kenerley CM. 93.  2010. Regulation of morphogenesis and biocontrol properties in Trichoderma virens by a VELVET protein, Vel1. Appl. Environ. Microbiol. 76:2345–52 [Google Scholar]
  94. Mukherjee PK, Latha J, Hadar R, Horwitz BA. 94.  2003. TmkA, a mitogen-activated protein kinase of Trichoderma virens, is involved in biocontrol properties and repression of conidiation in the dark. Eukaryot. Cell 2:446–55 [Google Scholar]
  95. Mukherjee PK, Mukhopadhyay A, Sarmah D, Shrestha S. 95.  1995. Comparative antagonistic properties of Gliocladium virens and Trichoderma harzianum on Sclerotium rolfsii and Rhizoctonia solani: its relevance to understanding the mechanisms of biocontrol. J. Phytopathol. 143:275–79 [Google Scholar]
  96. Mukherjee PK, Wiest A, Ruiz N, Keightley A, Moran-Diez ME. 96.  et al. 2011. Two classes of new peptaibols are synthesized by a single non-ribosomal peptide synthetase of Trichoderma virens. J. Biol. Chem. 286:4544–54 [Google Scholar]
  97. Munoz G, Nakari-Setala T, Agosin E, Penttila M. 97.  1997. Hydrophobin gene srh1, expressed during sporulation of the biocontrol agent Trichoderma harzianum. Curr. Genet. 32:225–30 [Google Scholar]
  98. Papavizas GC. 98.  1985. Trichoderma and Gliocladium: biology, ecology, and potential for biocontrol. Annu. Rev. Phytopathol. 23:23–54 [Google Scholar]
  99. Park G, Colot HV, Collopy PD, Krystofova S, Crew C. 99.  et al. 2011. High-throughput production of gene replacement mutants in Neurospora crassa. Methods Mol. Biol. 722:179–89 [Google Scholar]
  100. Penttila M, Nevalainen H, Ratto M, Salminen E, Knowles J. 100.  1987. A versatile transformation system for the cellulolytic filamentous fungus Trichoderma reesei. Gene 61:155–64 [Google Scholar]
  101. Reithner B, Brunner K, Schuhmacher R, Peissl I, Seidl V. 101.  et al. 2005. The G protein alpha subunit Tga1 of Trichoderma atroviride is involved in chitinase formation and differential production of antifungal metabolites. Fungal Genet. Biol. 42:749–60 [Google Scholar]
  102. Reithner B, Ibarra-Laclette E, Mach RL, Herrera-Estrella A. 102.  2011. Identification of mycoparasitism-related genes in Trichoderma atroviride. Appl. Environ. Microbiol. 77:4361–70 [Google Scholar]
  103. Rocha-Ramirez V, Omero C, Chet I, Horwitz BA, Herrera-Estrella A. 103.  2002. Trichoderma atroviride G-protein α-subunit gene tga1 is involved in mycoparasitic coiling and conidiation. Eukaryot. Cell 1:594–605 [Google Scholar]
  104. Ron M, Avni A. 104.  2004. The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16:1604–15 [Google Scholar]
  105. Rubio MB, Dominguez S, Monte E, Hermosa R. 105.  2012. Comparative study of Trichoderma gene expression in interactions with tomato plants using high-density oligonucleotide microarrays. Microbiology 158:119–28 [Google Scholar]
  106. Rubio MB, Hermosa R, Reino JL, Collado IG, Monte E. 106.  2009. Thctf1 transcription factor of Trichoderma harzianum is involved in 6-pentyl-2H-pyran-2-one production and antifungal activity. Fungal Genet. Biol. 46:17–27 [Google Scholar]
  107. Samuels GJ, Chaverri P, Farr DF, McCray EB. 107.  2012. Trichoderma Online, Systematic Mycology and Microbiology Laboratory. Washington DC: USDA-ARS http://nt.ars-grin.gov/taxadescriptions/keys/TrichodermaIndex.cfm
  108. Schmoll M, Franchi L, Kubicek CP. 108.  2005. Envoy, a PAS/LOV domain protein of Hypocrea jecorina (anamorph Trichoderma reesei), modulates cellulase gene transcription in response to light. Eukaryot. Cell 4:1998–2007 [Google Scholar]
  109. Schmoll M, Schuster A, Silva Rdo N, Kubicek CP. 109.  2009. The G-α protein GNA3 of Hypocrea jecorina (anamorph Trichoderma reesei) regulates cellulase gene expression in the presence of light. Eukaryot. Cell 8:410–20 [Google Scholar]
  110. Schmoll M, Seibel C, Tisch D, Dorrer M, Kubicek CP. 110.  2010. A novel class of peptide pheromone precursors in ascomycetous fungi. Mol. Microbiol. 77:1483–501 [Google Scholar]
  111. Schuster A, Bruno KS, Collett JR, Baker SE, Seiboth B. 111.  et al. 2012. A versatile toolkit for high throughput functional genomics with Trichoderma reesei. Biotechnol. Biofuels 5:1 [Google Scholar]
  112. Schuster A, Tisch D, Seidl-Seiboth V, Kubicek CP, Schmoll M. 112.  2012. Roles of protein kinase A and adenylate cyclase in light-modulated cellulase regulation in Trichoderma reesei. Appl. Environ. Microbiol. 78:2168–78 [Google Scholar]
  113. Segarra G, Casanova E, Bellido D, Odena MA, Oliveira E, Trillas I. 113.  2007. Proteome, salicylic acid, and jasmonic acid changes in cucumber plants inoculated with Trichoderma asperellum strain T34. Proteomics 7:3943–52 [Google Scholar]
  114. Segarra G, Van der Ent S, Trillas I, Pieterse CM. 114.  2009. MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biol.(Stuttg.) 11:90–96 [Google Scholar]
  115. Seibel C, Gremel G, do Nascimento Silva R, Schuster A, Kubicek CP, Schmoll M. 115.  2009. Light-dependent roles of the G-protein α subunit GNA1 of Hypocrea jecorina (anamorph Trichoderma reesei). BMC Biol. 7:58 [Google Scholar]
  116. Seibel C, Tisch D, Kubicek CP, Schmoll M. 116.  2012. ENVOY is a major determinant in regulation of sexual development in Hypocrea jecorina (Trichoderma reesei). Eukaryot. Cell 11:885–95 [Google Scholar]
  117. Seibel C, Tisch D, Kubicek CP, Schmoll M. 117.  2012. The role of pheromone receptors for communication and mating in Hypocrea jecorina (Trichoderma reesei). Fungal Genet. Biol. 49:814–24 [Google Scholar]
  118. Seiboth B, Ivanova C, Seidl-Seiboth V. 118.  2011. Trichoderma reesei: a fungal enzyme producer for cellulosic biofuels. Biofuel Production: Recent Developments and Prospects M dos Santos Bernardes 309–40 Rijeka, Croatia: Intech [Google Scholar]
  119. Seiboth B, Karimi RA, Phatale PA, Linke R, Hartl L. 119.  et al. 2012. The putative protein methyltransferase LAE1 controls cellulase gene expression in Trichoderma reesei. Mol. Microbiol. 84:1150–64 [Google Scholar]
  120. Seiboth B, Herold S, Kubicek CP. 120.  2012. Metabolic engineering of inducer formation for cellulase and hemicellulase gene expression in Trichoderma reesei. Subcell. Biochem 64:367–90 [Google Scholar]
  121. Seidl V, Marchetti M, Schandl R, Allmaier G, Kubicek CP. 121.  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. 273:4346–59 [Google Scholar]
  122. Seidl V, Seibel C, Kubicek CP, Schmoll M. 122.  2009. Sexual development in the industrial workhorse Trichoderma reesei. Proc. Natl. Acad. Sci. USA 106:13909–14 [Google Scholar]
  123. Seidl V, Song L, Lindquist E, Gruber S, Koptchinskiy A. 123.  et al. 2009. Transcriptomic response of the mycoparasitic fungus Trichoderma atroviride to the presence of a fungal prey. BMC Genomics 10:567 [Google Scholar]
  124. Shoemaker S, Schweikart V, Ladner M, Gelfand D, Kwok S. 124.  et al. 1983. Molecular cloning of exo-cellubiohydrolase I derived from Trichoderma reesei strain L27. Nat. Biotechnol. 1:691–96 [Google Scholar]
  125. Shoresh M, Gal-On A, Leibman D, Chet I. 125.  2006. Characterization of a mitogen-activated protein kinase gene from cucumber required for Trichoderma-conferred plant resistance. Plant Physiol. 142:1169–79 [Google Scholar]
  126. Shoresh M, Harman GE, Mastouri F. 126.  2010. Induced systemic resistance and plant responses to fungal biocontrol agents. Annu. Rev. Phytopathol. 48:21–43 [Google Scholar]
  127. Son H, Seo YS, Min K, Park AR, Lee J. 127.  et al. 2011. A phenome-based functional analysis of transcription factors in the cereal head blight fungus, Fusarium graminearum. PLoS Pathog. 7:e1002310 [Google Scholar]
  128. Steyaert JM, Weld RJ, Mendoza-Mendoza A, Stewart A. 128.  2010. Reproduction without sex: conidiation in the filamentous fungus Trichoderma. Microbiology 156:2887–900 [Google Scholar]
  129. Steyaert JM, Weld RJ, Stewart A. 129.  2010. Ambient pH intrinsically influences Trichoderma conidiation and colony morphology. Fungal Biol. 114:198–208 [Google Scholar]
  130. Stricker AR, Grosstessner-Hain K, Wurleitner E, Mach RL. 130.  2006. Xyr1 (xylanase regulator 1) regulates both the hydrolytic enzyme system and D-xylose metabolism in Hypocrea jecorina. Eukaryot. Cell 5:2128–37 [Google Scholar]
  131. Tisch D, Kubicek CP, Schmoll M. 131.  2011. New insights into the mechanism of light modulated signaling by heterotrimeric G-proteins: ENVOY acts on gna1 and gna3 and adjusts cAMP levels in Trichoderma reesei (Hypocrea jecorina). Fungal Genet. Biol. 48:631–40 [Google Scholar]
  132. Tisch D, Schmoll M. 132.  2010. Light regulation of metabolic pathways in fungi. Appl. Microbiol. Biotechnol. 85:1259–77 [Google Scholar]
  133. Vargas WA, Crutcher FK, Kenerley CM. 133.  2011. Functional characterization of a plant-like sucrose transporter from the beneficial fungus Trichoderma virens. Regulation of the symbiotic association with plants by sucrose metabolism inside the fungal cells. New Phytol. 189:777–89 [Google Scholar]
  134. Vargas WA, Mandawe JC, Kenerley CM. 134.  2009. Plant-derived sucrose is a key element in the symbiotic association between Trichoderma virens and maize plants. Plant Physiol. 151:792–808 [Google Scholar]
  135. Velazquez-Robledo R, Contreras-Cornejo H, Macias-Rodriguez LI, Hernandez-Morales A, Aguirre J. 135.  et al. 2011. Role of the 4-phosphopantetheinyl transferase of Trichoderma virens in secondary metabolism, and induction of plant defense responses. Mol. Plant-Microbe Interact. 24:1459–71 [Google Scholar]
  136. Verma M, Brar S, Tyagi R, Surampalli R, Valero J. 136.  2007. Antagonistic fungi, Trichoderma spp.: panoply of biological control. Biochem. Eng. J. 37:1–20 [Google Scholar]
  137. Viterbo A, Harel M, Horwitz BA, Chet I, Mukherjee PK. 137.  2005. Trichoderma mitogen-activated protein kinase signaling is involved in induction of plant systemic resistance. Appl. Environ. Microbiol. 71:6241–46 [Google Scholar]
  138. Viterbo A, Horwitz BA. 138.  2010. Mycoparasitism. Cellular and Molecular Biology of Filamentous Fungi K Borkovich, DJ Ebbole 676–93 Washington, DC: ASM Press [Google Scholar]
  139. Vitikainen M, Arvas M, Pakula T, Oja M, Penttila M, Saloheimo M. 139.  2010. Array comparative genomic hybridization analysis of Trichoderma reesei strains with enhanced cellulase production properties. BMC Genomics 11:441 [Google Scholar]
  140. Vizcaino JA, Redondo J, Suarez MB, Cardoza RE, Hermosa R. 140.  et al. 2007. Generation, annotation, and analysis of ESTs from four different Trichoderma strains grown under conditions related to biocontrol. Appl. Microbiol. Biotechnol. 75:853–62 [Google Scholar]
  141. Weindling R. 141.  1932. Trichoderma lignorum as a parasite of other soil fungi. Phytopathology 22:837–45 [Google Scholar]
  142. Weindling R. 142.  1934. Studies on a lethal principle effective in the parasitic action of Trichoderma lignorum on Rhizoctonia solani and other soil fungi. Phytopathology 24:1153–79 [Google Scholar]
  143. Wells H, Bell D, Jaworski A. 143.  1972. Efficacy of Trichoderma harzianum as a biological control for Sclerotium rolfsii. Phytopathology 62:442–47 [Google Scholar]
  144. Wiest A, Grzegorski D, Xu BW, Goulard C, Rebuffat S. 144.  et al. 2002. Identification of peptaibols from Trichoderma virens and cloning of a peptaibol synthetase. J. Biol. Chem. 277:20862–68 [Google Scholar]
  145. Yedidia I, Benhamou N, Chet I. 145.  1999. Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl. Environ. Microbiol. 65:1061–70 [Google Scholar]
  146. Zamioudis C, Pieterse CM. 146.  2012. Modulation of host immunity by beneficial microbes. Mol. Plant-Microbe Interact. 25:139–50 [Google Scholar]
  147. Zhang J, Zhang Y, Zhong Y, Qu Y, Wang T. 147.  2012. Ras GTPases modulate morphogenesis, sporulation and cellulase gene expression in the cellulolytic fungus Trichoderma reesei. PLoS ONE 7:e48786 [Google Scholar]
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Trichoderma Research in the Genome Era
Annual Review of Phytopathology 51, 105 (2013); https://doi.org/10.1146/annurev-phyto-082712-102353
/content/journals/10.1146/annurev-phyto-082712-102353
/content/journals/10.1146/annurev-phyto-082712-102353
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Supplemental Material

Supplementary Data

  • Download all Supplemental Materials as a PDF. Includes Supplemental Table 1: A summary of some features of the sequenced genomes and Supplemental Figure 1: PKS-NRPS gene clusters of Trichoderma spp. (also reproduced below).

    Supplemental Figure 1: PKS-NRPS gene clusters of Trichoderma spp.

  • Article Type: Review Article

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