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Trichoderma: the genomics of opportunistic success

A Corrigendum to this article was published on 24 October 2011

Key Points

  • Trichoderma is a genus of filamentous fungi that display a range of lifestyles and interactions with other fungi, animals and plants.Because of their ability to antagonize plant-pathogenic fungi and to stimulate plant growth and defence, some Trichoderma strains are used for biological control of plant diseases.

  • A recent comparative analysis of the genomes from Trichoderma reesei, Trichoderma virens and Trichoderma atroviride (known as Hypocrea jecorina, Hypocrea virens and Hypocrea atroviridis in their respective teleomorphic (sexual) forms) has revealed that mycotrophy seems to be an ancient trait of the genus, as illustrated by an amplification of several gene families that encode proteins and enzymes involved in antagonism and killing of other fungi.

  • Mycotrophy and various forms of parasitism on other fungi (mycoparasitism), combined with broad environmental opportunism, seem to have driven the evolution of the present interactions of Trichoderma spp. with plants and animals. The presence of potential fungal prey and plant root-derived nutrients in the plant rhizosphere may have been major attractors for the colonization of the rhizosphere by Trichoderma spp. ancestors.

  • The phylogeny of Trichoderma strains suggests that endophytic strains and strains that are facultative pathogens of humans have recently evolved towards these new niches (that is, plant and animal tissues). This evolution may have been facilitated by the presence of genes that enable effective competition and opportunism.

Abstract

Trichoderma is a genus of common filamentous fungi that display a remarkable range of lifestyles and interactions with other fungi, animals and plants. Because of their ability to antagonize plant-pathogenic fungi and to stimulate plant growth and defence responses, some Trichoderma strains are used for biological control of plant diseases. In this Review, we discuss recent advances in molecular ecology and genomics which indicate that the interactions of Trichoderma spp. with animals and plants may have evolved as a result of saprotrophy on fungal biomass (mycotrophy) and various forms of parasitism on other fungi (mycoparasitism), combined with broad environmental opportunism.

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Figure 1: Mycotrophy of Hypocrea/Trichoderma spp.
Figure 2: Mycoparasitism of Hypocrea/Trichoderma spp. within the soil community.
Figure 3: Mycotrophy of Hypocrea atroviridis/Trichoderma atroviridae.
Figure 4: Interactions of Hypocrea/Trichoderma spp. with other organisms in the rhizosphere.

References

  1. Klein, D. & Eveleigh, D. E. In: Trichoderma and Gliocladium Vol.1 (eds Kubicek, C. P. & Harman, G. E.), 57–69 (Taylor and Francis, London, 1998).

    Google Scholar 

  2. Brotman, Y., Kapuganti, J. G. & Viterbo, A. Trichoderma. Curr. Biol. 20, R390–R391 (2010).

    Article  CAS  PubMed  Google Scholar 

  3. Jaklitsch, W. M. European species of Hypocrea Part I. The green-spored species. Stud. Mycol. 63, 1–91 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  4. Jaklitsch, W. M. European species of Hypocrea Part II: species with hyaline ascospores. Fungal Divers. 48, 1–247 (2011). Together with reference 3, this provides an excellent survey of the diversity and ecology of Hypocrea/Trichoderma spp.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Druzhinina, I. S., Kubicek, C. P., Komo´n-Zelazowska, M., Mulaw, T. B. & Bissett, J. The Trichoderma harzianum demon: complex speciation history resulting in coexistence of hypothetical biological species, recent agamospecies and numerous relict lineages. BMC Evol. Biol. 10, 94 (2010). This paper highlights the diversity and evolution of the T . cf. harzianum species complex.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Druzhinina, I. S., Komo´n-Zelazowska, M., Atanasova, L., Seidl, V. & Kubicek, C. P. Evolution and ecophysiology of the industrial producer Hypocrea jecorina (anamorph Trichoderma reesei) and a new sympatric agamospecies related to it. PLoS ONE 5, e9191 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Druzhinina, I. S. et al. Alternative reproductive strategies of Hypocrea orientalis and genetically close but clonal Trichoderma longibrachiatum, both capable of causing invasive mycoses of humans. Microbiology 154, 3447–3459 (2008). This work shows that T. longibrachiatum and H. orientalis are two different species with different reproduction strategies, and that both species can cause invasive mycoses.

    Article  CAS  PubMed  Google Scholar 

  8. Samuels, G. J., Ismaiel, A., Bon, M. C., De Respinis, S. & Petrini, O. Trichoderma asperellum sensu lato consists of two cryptic species. Mycologia 102, 944–966 (2010).

    Article  CAS  PubMed  Google Scholar 

  9. Kubicek, C. P., Komon-Zelazowska, M. & Druzhinina, I. S. Fungal genus Hypocrea/Trichoderma: from barcodes to biodiversity. J. Zhejiang Univ. Sci. B 9, 753–763 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Druzhinina, I. S., Kopchinskiy, A. & Kubicek, C. P. The first 100 Trichoderma species characterized by molecular data. Mycoscience 47, 55–64 (2006).

    Article  CAS  Google Scholar 

  11. Elad, Y., Barak, R. & Chet, I. Parasitism of sclerotia of Sclerotium rolfsii by Trichoderma harzianum. Soil Biol. Biochem. 16, 381–386 (1984).

    Article  CAS  Google Scholar 

  12. Rossmann, A. Y., Samuels, G. J., Rogerson, C. T. & Lowen, R. Genera of Bionectriaceae, Hypocreaceae and Nectriaceae (Hyprocrealses, Ascomycetes). Stud. Mycol. 42, 1–83 (1999).

    Google Scholar 

  13. Kubicek, C. P. et al. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol. 12, R40 (2011). A comparative analysis of the genomes of H. jecorina, H. virens and H. atroviridis , highlighting the gene repertoire that is related to mycoparasitism.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Martinez, D. et al. Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nature Biotech. 26, 553–560 (2008).

    Article  CAS  Google Scholar 

  15. Benítez, T., Rincón, A. M., Limón, M. C. & Codón, A. C. Biocontrol mechanisms of Trichoderma strains. Int. Microbiol. 7, 249–260 (2004).

    PubMed  Google Scholar 

  16. Howell, C. R. Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis. 87, 4–10 (2003).

    Article  CAS  PubMed  Google Scholar 

  17. Harman, G. E. Multifunctional fungal plant symbionts: new tools to enhance plant growth and productivity. New Phytol. 189, 647–649 (2011).

    Article  PubMed  Google Scholar 

  18. Harman, G. E., Howell, C. R., Viterbo, A., Chet, I. & Lorito, M. Trichoderma species—opportunistic, avirulent plant symbionts. Nature Rev. Microbiol. 2, 43–56 (2004).

    Article  CAS  Google Scholar 

  19. Lorito, M., Woo, S. L., Harman, G. E. & Monte, E. Translational research on Trichoderma: from 'omics to the field. Annu. Rev. Phytopathol. 48, 395–417 (2010).

    Article  CAS  PubMed  Google Scholar 

  20. Seidl, V. et al. Transcriptomic response of the mycoparasitic fungus Trichoderma atroviride to the presence of a fungal prey. BMC Genomics 10, 567 (2009). This study identifies genes that are upregulated in H. atroviridis during its antagonistic interaction with plant-pathogenic fungi.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Suárez, M. B., Vizcaíno, J. A., Llobell, A. & Monte, E. Characterization of genes encoding novel peptidases in the biocontrol fungus Trichoderma harzianum CECT 2413 using the TrichoEST functional genomics approach. Curr. Genet. 51, 331–342 (2007).

    Article  CAS  PubMed  Google Scholar 

  22. Flores, A., Chet, I. & Herrera-Estrella, A. Improved biocontrol activity of Trichoderma harzianum by over-expression of the proteinase-encoding gene prb1. Curr. Genet. 31, 30–37 (1997).

    Article  CAS  PubMed  Google Scholar 

  23. Dijksterhuis, J., Veenhuis, M., Harder, W. & Nordbring-Hertz, B. Nematophagous fungi: physiological aspects and structure–function relationships. Adv. Microb. Physiol. 36, 111–143 (1994).

    Article  CAS  PubMed  Google Scholar 

  24. Omann, M. et al. A cAMP receptor-like GPCR is involved in Trichoderma atroviride mycoparasitism. IOBC/WPRS Bull. 43, 105–108 (2009).

    Google Scholar 

  25. Rocha-Ramirez, V. et al. Trichoderma atroviride G.-protein α-subunit gene tga1 is involved in mycoparasitic coiling and conidiation. Eukaryot. Cell 1, 594–605 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Reithner, B. et al. The G protein α subunit Tga1 of Trichoderma atroviride is involved in chitinase formation and differential production of antifungal metabolites. Fungal Genet. Biol. 42, 749–760 (2004).

    Article  CAS  Google Scholar 

  27. Mukherjee, P. K., Latha, J., Hadar, R. & Horwitz, B. A. Role of two G-protein alpha subunits, TgaA and TgaB, in the antagonism of plant pathogens by Trichoderma virens. Appl. Environ. Microbiol. 70, 542–549 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Schmoll, M. The information highways of a biotechnological workhorse—signal transduction in Hypocrea jecorina. BMC Genomics 9, 430 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Mukherjee, P., Latha, J., Hadar, R. & Horwitz, B. A. TmkA, a mitogen-activated protein kinase of Trichoderma virens, is involved in biocontrol properties and repression of conidiation in the dark. Eukaryot. Cell 2, 446–455 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Viterbo, A., Harel, M., Horwitz, B. A., Chet, I. & Mukherjee, P. K. Trichoderma mitogen-activated protein kinase signaling is involved in induction of plant systemic resistance. Appl. Environ. Microbiol. 71, 6241–6246 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Mendoza-Mendoza, A. et al. The MAP kinase TVK1 regulates conidiation, hydrophobicity and the expression of genes encoding cell wall proteins in the fungus Trichoderma virens. Microbiology 153, 2137–2147 (2007).

    Article  CAS  PubMed  Google Scholar 

  32. Reithner, B. et al. Signaling via the Trichoderma atroviride mitogen-activated protein kinase Tmk1 differentially affects mycoparasitism and plant protection. Fungal Genet. Biol. 44, 1123–1133 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Kumar, A. et al. 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, 765–770 (2010).

    Article  CAS  PubMed  Google Scholar 

  34. Delgado-Jarana, J., Sousa, S., González, F., Rey, M. & Llobell, A. ThHog1 controls the hyperosmotic response in Trichoderma harzianum. Microbiology 162, 1687–1700 (2006).

    Article  CAS  Google Scholar 

  35. Inbar, J. & Chet, I. The role of lectins in recognition and adhesion of the mycoparasitic fungus Trichoderma spp. to its host. Adv. Exp. Med. Biol. 408, 229–231 (1996).

    Article  CAS  PubMed  Google Scholar 

  36. Lu, Z. et al. In vivo study of Trichoderma-pathogen-plant interactions, using constitutive and inducible green fluorescent protein reporter systems. Appl. Environ. Microbiol. 70, 3073–3081 (2004). This investigation monitors the antagonism of H. atroviridis against plant-pathogenic fungi directly in soil.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Chacón, M. R. et al. Microscopic and transcriptome analyses of early colonization of tomato roots by Trichoderma harzianum. Int. Microbiol. 10, 19–27 (2007).

    PubMed  Google Scholar 

  38. de Jong, J. C., McCormack, B. J., Smirnoff, N. & Talbot, N. J. Glycerol generates turgor in rice blast. Nature 389, 244–245 (1997).

    Article  CAS  Google Scholar 

  39. Kubicek, C. P., Baker, S., Gamauf, C., Kenerley, C. M. & Druzhinina, I. S. Purifying selection and birth-and-death evolution in the class II hydrophobin gene families of the ascomycete Trichoderma/Hypocrea. BMC Evol. Biol. 8, 4 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Papapostolou, I. & Georgiou, C. D. Superoxide radical induces sclerotial differentiation in filamentous phytopathogenic fungi: a superoxide dismutase mimetics study. Microbiology 156, 960–966 (2010).

    Article  CAS  PubMed  Google Scholar 

  41. Aliferis, K. A. & Jabaji, S. Metabolite composition and bioactivity of Rhizoctonia solani sclerotial exudates. J. Agric. Food Chem. 58, 7604–7615 (2010).

    Article  CAS  PubMed  Google Scholar 

  42. Ruocco, M. et al. Identification of a new biocontrol gene in Trichoderma atroviride: the role of an ABC transporter membrane pump in the interaction with different plant-pathogenic fungi. Mol. Plant Microbe Interact. 22, 291–301 (2009).

    Article  CAS  PubMed  Google Scholar 

  43. Latgé, J. P. The cell wall: a carbohydrate armour for the fungal cell. Mol. Microbiol. 66, 279–290 (2007).

    Article  CAS  PubMed  Google Scholar 

  44. Seidl, V. Chitinases of filamentous fungi: a large group of diverse proteins with multiple physiological functions. Fungal Biol. Rev. 22, 36–42 (2008). This article describes the diversity of chitinases from Hypocrea/Trichoderma spp. and other filamentous fungi.

    Article  Google Scholar 

  45. Limón, M. C. et al. Increased antifungal and chitinase specific activities of Trichoderma harzianum CECT 2413 by addition of a cellulose binding domain. Appl. Microbiol. Biotechnol. 64, 675–685 (2004).

    Article  CAS  PubMed  Google Scholar 

  46. Ihrmark, K. et al. Comparative molecular evolution of Trichoderma chitinases in response to mycoparasitic interactions. Evol. Bioinform. Online 6, 1–26 (2010). This paper provides evidence for positive selection of some chitinases in mycoparasitic Hypocrea/Trichoderma spp.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Montero, M., Sanz, L., Rey, M., Llobell, A. & Monte, E. Cloning and characterization of bgn16·3, coding for a β-1,6-glucanase expressed during Trichoderma harzianum mycoparasitism. J. Appl. Microbiol. 103, 1291–1300 (2007).

    Article  CAS  PubMed  Google Scholar 

  48. Djonovic, S., Pozo, M. J. & Kenerley, C. M. Tvbgn3, a β-1,6-glucanase from the biocontrol fungus Trichoderma virens, is involved in mycoparasitism and control of Pythium ultimum. Appl. Environ. Microbiol. 72, 7661–7670 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Casas-Flores, S. E. & Herrera-Estrella, A. in The Mycota, Environmental and Microbial Relationships 2nd edn Vol. 4, 159–187 (Springer Berlin-Heidelberg, New York, 2007).

    Google Scholar 

  50. Bird, A. F. & Bird, J. The Structure of Nematodes. (Academic Press, San Diego & London, 1991).

    Google Scholar 

  51. Sharon, E. et al. Biological control of the root-knot nematode Meloidogyne javanica by Trichoderma harzianum. Phytopathology 91, 687–693 (2001).

    Article  CAS  PubMed  Google Scholar 

  52. Suarez, B., Rey, M., Castillo, P., Monte, E. & Llobell, A. Isolation and characterization of PRA1, a trypsin-like protease from the biocontrol agent Trichoderma harzianum CECT 2413 displaying nematicidal activity. Appl. Microbiol. Biotechnol. 65, 46–55 (2004).

    Article  CAS  PubMed  Google Scholar 

  53. Chen, L. L. et al. Characterization and gene cloning of a novel serine protease with nematicidal activity from Trichoderma pseudokoningii SMF2. FEMS Microbiol. Lett. 299, 135–142 (2009).

    Article  CAS  PubMed  Google Scholar 

  54. Kredics, L. et al. Clinical importance of the genus Trichoderma. A review. Acta Microbiol. Immunol. Hung. 50, 105–117 (2003).

    Article  CAS  PubMed  Google Scholar 

  55. Kratzer, C., Tobudic, S., Schmoll, M., Graninger, W. & Georgopoulos, A. In vitro activity and synergism of amphotericin B, azoles and cationic antimicrobials against the emerging pathogen Trichoderma spp. J. Antimicrob. Chemother. 58, 1058–1061 (2006).

    Article  CAS  PubMed  Google Scholar 

  56. Seibel, C. et al. PR4.5: Pathogenesis related gene expression in the opportunistic fungal pathogen Trichoderma longibrachiatum. 9th European Conference in Fungal Genetics — Meeting Abstracts [online], (2008).

    Google Scholar 

  57. Mulaw, T. B., Kubicek, C. P. & Druzhinina, I. S. The rhizosphere of Coffea arabica in its native highland forests of Ethiopia is associated with a distinguished diversity of Trichoderma. Diversity 2, 527–549 (2010).

    Article  CAS  Google Scholar 

  58. Migheli, Q. et al. Soils of a Mediterranean hot spotof biodiversity and endemism (Sardinia, Tyrrhenian Islands) are inhabited by pan-European, invasive species of Hypocrea/Trichoderma. Environ. Microbiol. 11, 35–46 (2009).

    Article  CAS  PubMed  Google Scholar 

  59. Calvet, C., Pera, J. & Barea, J. M. Growth response of marigold (Tagetes erecta L.) to inoculation with Glomus mosseae, Trichoderma aureoviride and Pythium ultimum in a peat-perlite mixture. Plant Soil 148, 1–6 (1993).

    Article  Google Scholar 

  60. Datnoff, L. E., Nemec, S. & Pernezny, K. Biological control of fusarium crown and root rot of tomato in Florida using Trichoderma harzianum and Glomus intraradices. Biol. Control 5, 427–431 (1995).

    Article  Google Scholar 

  61. McAllister, C. B., García-Romera, I., Godeas, A. & Ocampo, J. A. Interactions between Trichoderma koningii, Fusarium solani and Glomus mosseae: effects on plant growth, arbuscular mycorrhizas and the saprophyte inoculants. Soil Biol. Biochem. 26, 1363–1367 (1994).

    Article  Google Scholar 

  62. Nemec, S., Datnoff, L. E., Strandberg, J. Efficacy of biocontrol agents in planting mixes to colonize plant roots and control root diseases of vegetables and citrus. Crop Prot. 15, 735–742 (1996).

    Article  Google Scholar 

  63. Siddiqui, Z. A. & Mohmood, I. Biological control of Heterodera cajani and Fusarium udum on pigeonpea by Glomus mosseae, Trichoderma harzianum, and Verticillium chlamydosporium. Isr. J. Plant Sci. 44, 49–56 (1996).

    Article  Google Scholar 

  64. Green, H., Larsen, J., Olsson, P. A., Jensen, D. F. & Jakobsen, I. I. Suppression of the biocontrol agent Trichoderma harzianum by mycelium of the arbuscular mycorrhizal fungus Glomus intraradices in root-free soil. Appl. Environ. Microbiol. 65, 1428–1434 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Werner, A. & Zadworny, M. In vitro evidence of mycoparasitism of the ectomycorrhizal fungus Laccaria laccata against Mucor hiemalis in the rhizosphere of Pinus sylvestris. Mycorrhiza 13, 41–47 (2003).

    Article  PubMed  Google Scholar 

  66. Moran-Diez, E. et al. The ThPG1 endopolygalacturonase is required for the Trichoderma harzianum–plant beneficial interaction. Mol. Plant Microbe Interact. 22, 1021–1031 (2009).

    Article  CAS  PubMed  Google Scholar 

  67. Nehls, U., Göhringer, F., Wittulsky, S. & Dietz, S. Fungal carbohydrate support in the ectomycorrhizal symbiosis: a review. Plant Biol. (Stuttg.) 12, 292–301 (2010).

    Article  CAS  Google Scholar 

  68. Vargas, W. A., Mandawe, J. C. & Kenerley, C. M. Plant-derived sucrose is a key element in the symbiotic association between Trichoderma virens and maize plants. Plant Physiol. 151, 792–808 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Vargas, W. A., Crutcher, F. K. & Kenerley, C. M. 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, 777–789 (2011). This paper shows that H. virens can use plant-derived sucrose.

    Article  CAS  PubMed  Google Scholar 

  70. Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323–329 (2006).

    Article  CAS  PubMed  Google Scholar 

  71. Shoresh, M., Harman, G. E. & Mastouri, F. Induced systemic resistance and plant responses to fungal biocontrol agents. Annu. Rev. Phytopathol. 48, 21–43 (2010). This review summarizes how fungi that are used as biocontrol agents stimulate the plant response.

    Article  CAS  PubMed  Google Scholar 

  72. Yedidia, I. I., Benhamou, N. & Chet, I. Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl. Environ. Microbiol. 65, 1061–1070 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Segarra, G. et al. Proteome, salicylic acid, and jasmonic acid changes in cucumber plants inoculated with Trichoderma asperellum strain T34. Proteomics 7, 3943–3952 (2007).

    Article  CAS  PubMed  Google Scholar 

  74. Dean, J. F. & Anderson, J. D. Ethylene biosynthesis-inducing xylanase: II. purification and physical characterization of the enzyme produced by Trichoderma viride. Plant Physiol. 95, 316–323 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Hanson, L. E. & Howell, C. R. Elicitors of plant defense responses from biocontrol strains of Trichoderma virens. Phytopathol. 94, 171–176 (2004).

    Article  CAS  Google Scholar 

  76. Enkerli, J., Felix, G. & Boller, T. The enzymatic activity of fungal xylanase is not necessary for its elicitor activity. Plant Physiol. 121, 391–397 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Sharon, A., Fuchs, Y. & Anderson, J. D. The elicitation of ethylene biosynthesis by a Trichoderma xylanase is not related to the cell wall degradation activity of the enzyme. Plant Physiol. 102, 1325–1329 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Ron, M. & Avni, A. The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16, 1604–1615 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Bar, M. & Avni, A. EHD2 inhibits ligand-induced endocytosis and signaling of the leucine-rich repeat receptor-like protein LeEix2. Plant J. 59, 600–611 (2009).

    Article  CAS  PubMed  Google Scholar 

  80. Bailey, B. A., Korcak, R. F. & Anderson, J. D. Alterations in Nicotiana tabacum L. cv xanthi cell membrane function following treatment with an ethylene biosynthesis-inducing endoxylanase. Plant Physiol. 100, 749–755 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Viterbo, A., Wiest, A., Brotman, Y., Chet, I. & Kenerley, C. M. The 18mer peptaibols from Trichoderma virens elicit plant defence responses. Mol. Plant Pathol. 8, 737–746 (2007). This work demonstrates that peptaibols can induce a plant response.

    Article  CAS  PubMed  Google Scholar 

  82. Saloheimo, M. et al. Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials. Eur. J. Biochem. 269, 4202–4211 (2002).

    Article  CAS  PubMed  Google Scholar 

  83. Brotman, Y., Briff, E., Viterbo, A. & Chet, I. Role of swollenin, an expansin-like protein from Trichoderma, in plant root colonization. Plant Physiol. 147, 779–789 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Guo, W. et al. Soybean β-expansin gene GmEXPB2 intrinsically involved in root system achitecture responses to abiotic stresses. Plant J. 66, 541–552 (2011).

    Article  CAS  PubMed  Google Scholar 

  85. Djonovic, S. et al. A proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol. 145, 875–889 (2007). This article describes the stimulation of ISR by a small cysteine-rich protein from H. virens.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Seidl, V., Marchetti, M., Schandl, R., Allmaier, G. & Kubicek, C. P. 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, 4346–4359 (2006).

    Article  CAS  PubMed  Google Scholar 

  87. Vargas, W. A., Djonovic, S., Sukno, S. A. & Kenerley, C. M. Dimerization controls the activity of fungal elicitors that trigger systemic resistance in plants. J. Biol. Chem. 283, 19804–19815 (2008).

    Article  CAS  PubMed  Google Scholar 

  88. Martin, F. et al. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452, 88–92 (2008).

    Article  CAS  PubMed  Google Scholar 

  89. Contreras-Cornejo, H. A., Macias-Rodriguez, L., Cortes-Penagos, C. & Lopez-Bucio, J. Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol. 149, 1579–1592 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Wang, K., Li, H. & Ecker, J. Ethylene biosynthesis and signaling networks. Plant Cell 14, S131–S151 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Viterbo, A., Landau, U., Kim, S., Chernin, L. & Chet, I. Characterization of ACC deaminase from the biocontrol and plant growth-promoting agent Trichoderma asperellum T203. FEMS Microbiol. Lett. 305, 42–48 (2010).

    Article  CAS  PubMed  Google Scholar 

  92. Glick, B. R. Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol. Lett. 251, 1–7 (2005).

    Article  CAS  PubMed  Google Scholar 

  93. Piotrowski, M. & Volmer, J. J. Cyanide metabolism in higher plants: cyanoalanine hydratase is a NIT4 homolog. Plant Mol. Biol. 61, 111–122 (2006).

    Article  CAS  PubMed  Google Scholar 

  94. Bae, H. et al. 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, 3279–3295 (2009). This paper provides evidence for the beneficial effects of T. hamatum , an endophytic species, to the plant.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Chaverri, P., Gazis, R. O. & Samuels, G. J. Trichoderma amazonicum, a new endophytic species on Hevea brasiliensis and H. guianensis from the Amazon basin. Mycologia 103, 139–151 (2011).

    Article  PubMed  Google Scholar 

  96. Samuels, G. J. et al. The Trichoderma koningii aggregate species. Stud. Mycol. 56, 67–133 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  97. Samuels, G. J. & Ismaiel, A. Trichoderma evansii and T. lieckfeldtiae: two new T. hamatum-like species. Mycologia 101, 142–152 (2009).

    Article  CAS  PubMed  Google Scholar 

  98. Rodriguez, R. J., White, J. F. Jr, Arnold, A. E. & Redman, R. S. Fungal endophytes: diversity and functional roles. New Phytol. 182, 314–330 (2009).

    Article  CAS  PubMed  Google Scholar 

  99. De Jaeger, N., Declerck, S. & de la Providencia, I. E. Mycoparasitism of arbuscular mycorrhizal fungi: a pathway for the entry of saprotrophic fungi into roots. FEMS Microbiol. Ecol. 73, 312–322 (2010). This study shows that mycoparasites can use mycorrhizal fungi to become endophytes.

    CAS  PubMed  Google Scholar 

  100. McNeill, J. et al. International Code of Botanical Nomenclature (Vienna Code) Adopted By the Seventeenth International Botanical Congress Vienna, Austria (Gantner, Ruggell, Liechtenstein, 2005).

  101. Kubicek, C. P., Komo´n-Zelazowska, M., Sándor, E. & Druzhinina, I. S. Facts and challenges in the understanding of the biosynthesis of peptaibols by Trichoderma. Chem. Biodivers. 4, 1068–1082 (2007).

    Article  CAS  PubMed  Google Scholar 

  102. Lorito, M., Farkas, V., Rebuffat, S., Bodo, B. & Kubicek, C. P. Cell wall synthesis is a major target of mycoparasitic antagonism by Trichoderma harzianum. J. Bacteriol. 178, 6382–6385 (1996).

    Article  CAS  PubMed  Google Scholar 

  103. Howell, C. R. Understanding the mechanisms employed by Trichoderma virens to effect biological control of cotton diseases. Phytopathology 96, 178–180 (2006).

    Article  PubMed  Google Scholar 

  104. Lumsden, R. D., Locke, J. C., Adkins, S. T., Walter, J. F. & Ridout, C. J. Isolation and localization of the antibiotic gliotoxin produced by Gliocladium virens from alginate prill in soil and soilless media. Phytopathology 82, 230–235 (1992).

    Article  CAS  Google Scholar 

  105. Howell, C. R., Stipanovic, R. & Lumsden, R. Antibiotic production by strains of Gliocladium virens and its relation to biocontrol of cotton seedling diseases. Biocontrol. Sci. Technol. 3, 435–441 (1993).

    Article  Google Scholar 

  106. Howell, C. R. & Stipanovic, R. D. Mechanisms in the biocontrol of Rhizoctonia solani-induced cotton seedling disease by Gliocladium virens: antibiosis. Phytopathology 85, 469–472 (1995).

    Article  Google Scholar 

  107. Howell, C. R. & Puckhaber, L. S. A study of the characteristics of “P” and “Q” strains of Trichoderma virens to account for differences in biological control efficacy against cotton seedling diseases. Biol. Control 33, 217–222 (2005).

    Article  Google Scholar 

  108. Jones, R. W. & Hancock, J. G. Conversion of viridin to viridiol by viridin-producing fungi. Can. J. Microbiol. 33, 963–966 (1987).

    Article  CAS  PubMed  Google Scholar 

  109. Mukherjee, M., Horwitz, B. A., Sherkhane, P. D., Hadar, R. & Mukherjee, P. K. 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 (2006).

    Article  CAS  PubMed  Google Scholar 

  110. Tijerino, A. et al. Overexpression of the trichodiene synthase gene tri5 increases trichodermin production and antimicrobial activity in Trichoderma brevicompactum. Fungal Genet. Biol. 48, 285–296 (2011).

    Article  CAS  PubMed  Google Scholar 

  111. Serrano-Carreon, L., Hathout, Y., Bensoussan, M. & Belin, J. M. Metabolism of linoleic acid or mevalonate and 6-pentyl-α-pyrone biosynthesis by Trichoderma species. Appl. Environ. Microbiol. 59, 2945–2950 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  112. Hanada, R. E. et al. Trichoderma martiale sp. nov., a new endophyte from sapwood of Theobroma cacao with a potential for biological control. Mycol. Res. 112, 1335–1343 (2008).

    Article  CAS  PubMed  Google Scholar 

  113. Samuels, G. J. et al. Trichoderma theobromicola and T. paucisporum: two new species isolated from cacao in South America. Mycol. Res. 110, 381–392 (2006).

    Article  PubMed  Google Scholar 

  114. Jaklitsch, W. M., Samuels, G. J., Dodd, S. L., Lu, B. S. & Druzhinina, I. S. Hypocrea rufa/Trichoderma viride: a reassessment, and description of five closely related species with and without warted conidia. Stud. Mycol. 56, 135–177 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  115. Zhang, C. L., Liu, S. P., Lin, F. C., Kubicek, C. P. & Druzhinina, I. S. Trichoderma taxi sp. nov., an endophytic fungus from Chinese yew Taxus mairei. FEMS Microbiol. Lett. 270, 90–96 (2007).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Work in the C.P.K., I.S.D., V.S.-S. and S.Z. laboratory (headed by C.P.K.) was supported by grants from the Austrian Science Foundation (P17895-B06, P20559, T390 and P-19340) and the Vienna Science and Technology Fund (WWTF LS09-036). The work of B.A.H., C.M.K. and P.K.M. was supported in part by grant TB-8031-08 from the Texas Department of Agriculture, USA, and the US–Israel Binational Agricultural Research and Development Fund.

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Glossary

Saprotrophic

Using extracellular digestion of dead or decayed organic matter as a food source.

Opportunistic

Able to rapidly adapt to occupy a newly arising ecological niche.

Biotrophic

Relying on another living organism for nutrition. This includes the broad spectrum of parasitic, mutualistic and commensalistic interactions.

Parasites

Organisms that take part in inter-species biotrophic interactions in which the parasites benefit at the expense of the other organisms in the interaction (the hosts).

Hemicellulolytic

Relating to the degradation of plant hemicelluloses such as xylans and pectins.

Nematophagous

Pertaining to fungi: specialized in trapping and digesting nematodes.

G protein-coupled receptors

(Guanine-nucleotide-binding protein-coupled receptors). Receptors that possess seven transmembrane helices, bind an extracellular signalling molecule and transmit this binding by activating a Gα subunit.

Lectins

Sugar-binding proteins that are highly specific for the respective sugar moiety and have a role in the recognition of cells and proteins.

Appressorium

A flattened hyphal pressing structure from which an infection peg emerges that enters the host.

Predation

An inter-organism association in which one organism affects another adversely and itself benefits from the interaction. A predator ultimately kills its prey and consumes all or part of the prey organism.

Mycoses

Fungal infections of animals or humans.

Mycorrhizal fungi

A group of fungi that establish symbiotic or weakly parasitic associations with the roots of vascular plants.

Induced systemic resistance

A process by which plants respond to a non-pathogenic microorganism, with a signalling cascade that is dependent on jasmonate and ethylene. This response leads to a long-lasting ability to mount a faster and stronger broad-spectrum defence when challenged by a pathogen. Both pathogen-associated molecular pattern-triggered immunity and effector-triggered immunity can lead to induced systemic resistance.

Ethylene

A gaseous, unsaturated hydrocarbon that acts as a plant hormone to promote growth and development and as an inhibiting stress factor.

Callose

A β-1,3-linked polysaccharide of the plant cell wall; this polysaccharide is formed in response to wounding (including infections by pathogens).

Systemic acquired resistance

A plant defence mechanism that is usually induced by exposure to a pathogen and confers long-lasting protection against a broad spectrum of microorganisms. It involves the production of the signal molecule salicylic acid, which then leads to the accumulation of pathogenesis-related proteins that are thought to contribute to resistance.

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Druzhinina, I., Seidl-Seiboth, V., Herrera-Estrella, A. et al. Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9, 749–759 (2011). https://doi.org/10.1038/nrmicro2637

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