, 47:55 | Cite as

The first 100 Trichoderma species characterized by molecular data

  • Irina S. Druzhinina
  • Alex G. Kopchinskiy
  • Christian P. Kubicek


Trichoderma species are generally abundant on decaying wood and in soil because of their success in various heterotrophic interactions, including decomposition, parasitism, and even opportunistic endophytism. Many Trichoderma species or, precisely, many individual Trichoderma strains, have various important applications in industry and human life, which led to the inclusion of Hypocrea jecorina (Trichoderma reesei), the well-known producer of industrial enzymes, in the list of organisms whose genomes have been sequenced. Trichoderma species also have been adopted as agents of biological control of plant pathogenic fungi and as antibiotic producers. Trichoderma longibrachiatum is known as an opportunistic pathogen of immunocompromised mammals, including humans, and some species are common indoor contaminants. Given these properties, correct identification at the species level is highly desirable. However, within the past decade, the number of recognized Trichoderma species has tripled, reaching 100. Therefore, Trichoderma taxonomy and species identification is a difficult issue. The abundant homoplasy in phenetic characters is likely the reason, given that the number of morphologically distinct species is significantly lower than the number of phylogenetically distinct species recognized using methods of gene sequence analysis. In this review, we introduce to the scientific community the development of modern tools for Trichoderma species identification: the oligonucleotide barcode program TrichOKEY version 1.0, and TrichoBLAST, the multilocus database of vouchered sequences powered by a similarity search tool. We also discuss the application of the Genealogic Concordance Phylogenetic Species Recognition approach. In combination, these advances make it possible to identify all known Trichoderma species based on sequence analysis.


  1. Abbott, EV 1927Taxonomic studies on soil fungiIowa State Coll J Sci11536Google Scholar
  2. Altschul, SF, Madden, TL, Schäffer, AA, Zhang, J, Zhang, Z, Miller, W, Lipman, DJ 1997Gapped BLAST and PSI-BLAST: a new generation of protein database search programsNucleic Acids Res2533893402CrossRefPubMedGoogle Scholar
  3. Bisby, GR 1939Trichoderma viride Pers. ex Fries, and notes on Hypocrea TransBr Mycol Soc23149168Google Scholar
  4. Bissett, J 1984A revision of the genus Trichoderma. I. Sect. Longibrachiatum sect. novCan J Bot62924931CrossRefGoogle Scholar
  5. Bissett, J 1991aA revision of the genus Trichoderma. II. Infrageneric classificationCan J Bot6923572372Google Scholar
  6. Bissett, J 1991bA revision of the genus Trichoderma. III. Sect. PachybasiumCan J Bot6923732417Google Scholar
  7. Bissett, J 1991cA revision of the genus Trichoderma. IV. Additional notes on section LongibrachiatumCan J Bot6924182420Google Scholar
  8. Bissett, J 1992Trichoderma atrovirideCan J Bot70639641Google Scholar
  9. Bissett, J, Szakacs, G, Nolan, CA, Druzhinina, IS, Kullnig-Gradinger, CM, Kubicek, CP 2003Seven new taxa of Trichoderma from AsiaCan J Bot81570586CrossRefGoogle Scholar
  10. Chaverri, P, Castlebury, LA, Samuels, GJ, Geiser, D 2003aMultilocus phylogenetic structure within the Trichoderma harzianum/Hypocrea lixii complexMol Phylogenet Evol27302313CrossRefGoogle Scholar
  11. Chaverri, P, Castlebury, LA, Overton, BE, Samuels, GJ 2003bHypocrea/Trichoderma: species with conidiophore elongations and green conidiaMycologia9511001140Google Scholar
  12. Chaverri, P, Samuels, GJ 2004Hypocrea/Trichoderma (Ascomycota, Hypocreales, Hypocreaceae): species with green ascosporesStud Mycol481116Google Scholar
  13. Cutler, HG, Cutler, SJ, Ross, SA, Sayed, KE, Dugan, FM, Bartlett, MG, Hill, AA, Hill, RA, Parker, SR 1999Koninginin G, a new metabolite from Trichoderma aureovirideJ Nat Prod62137139CrossRefPubMedGoogle Scholar
  14. Danielson, R, Davey, C 1973The abundance of Trichoderma propagules and the distribution of species in forest soilsSoil Biol Biochem5485494CrossRefGoogle Scholar
  15. de Queiroz, K 1992Phylogenetic definitions and taxonomic philosophyBiol Philos7295313CrossRefGoogle Scholar
  16. Druzhinina, I, Chaverri, P, Fallah, P, Kubicek, CP, Samuels, GJ 2004Hypocrea flaviconidia, a new species from Costa Rica with yellow conidiaStud Mycol50401407Google Scholar
  17. Druzhinina, I, Koptchinski, A, Komon, M, Bissett, J, Szakacs, G, Kubicek, CP 2005An oligonucleotide barcode for species identification in Trichoderma and HypocreaFungal Genet Biol42813828CrossRefPubMedGoogle Scholar
  18. Druzhinina, I, Kubicek, CP 2005Species concepts and biodiversity in Trichoderma and Hypocrea: from aggregate species to species clusters?J Zhejiang Univ Sci6100112CrossRefGoogle Scholar
  19. Gautheret, A, Dromer, F, Bourhis, JH, Andremont, A 1995Trichoderma pseudokoningii as a cause of fatal infection in a bone marrow transplant recipientClin Infect Dis2010631064PubMedGoogle Scholar
  20. Geiser, DM, Jiménez-Gasco, M, Kang, S, Makalowska, I, Veerarahavan, N, Ward, TJ, Zhang, N, Kuldau, GA, O'Donnell, K 2004FUSARIUM-ID v. 1.0: a DNA sequence database for identifying FusariumEur J Plant Pathol110473479CrossRefGoogle Scholar
  21. Gherbawy, Y, Druzhinina, I, Shaban, GM, Wuczkowsky, M, Yaser, M, El-Naghy, MA, Prillinger, HJ, Kubicek, CP 2004Trichoderma populations from alkaline agricultural soil in the Nile valley, Egypt, consist of only two speciesMycol Prog3211218CrossRefGoogle Scholar
  22. Harman, GE, Howell, CR, Viterbo, A, Chet, I, Lorito, M 2004Trichoderma species – opportunistic, avirulent plant symbiontsNat Rev Microbiol24356CrossRefPubMedGoogle Scholar
  23. Heckman, DS, Geiser, DM, Eidell, BR, Stauffer, RL, Kardos, NL, Hedges, SB 2001Molecular evidence for the early colonization of land by fungi and plantsScience29311291133CrossRefPubMedGoogle Scholar
  24. Hjeljord, L, Tronsmo, A 1998

    Trichoderma and Gliocladium in biological control: an overview

    Harman, GEKubicek, CP eds. Trichoderma and Gliocladium, vol 2. Enzymes, biological control and commercial applicationsTaylor & FrancisLondon131151
    Google Scholar
  25. Huelsenbeck, JP, Ronquist, F 2001MRBAYES: Bayesian inference of phylogenetic treesBioinformatics17754755CrossRefPubMedGoogle Scholar
  26. Humphris, SN, Bruce, A, Buultjens, E, Wheatley, RE 2002The effects of volatile microbial secondary metabolites on protein synthesis in Serpula lacrymansFEMS Microbiol Lett210215219PubMedGoogle Scholar
  27. Jaklitsch WM, Komon M, Kubicek CP, Druzhinina IS (2006) Hypocrea voglmayrii sp. nov. from the Austrian Alps represents a new phylogenetic clade in Hypocrea/Trichoderma. Mycologia in pressGoogle Scholar
  28. Kindermann, J, El-Ayouti, Y, Samuels, GJ, Kubicek, CP 1998Phylogeny of the genus Trichoderma based on sequence analysis of the internal transcribed spacer region 1 of the rDNA cladeFungal Genet Biol24298309CrossRefPubMedGoogle Scholar
  29. Klein, D, Eveleigh, DE 1998

    Ecology of Trichoderma

    Kubicek, CPHarman, GE eds. Trichoderma and Gliocladium, vol 1. Basic biology, taxonomy and geneticsTaylor & FrancisLondon5773
    Google Scholar
  30. Kopchinskiy, A, Komon, M, Kubicek, CP, Druzhinina, IS 2005TrichoBLAST: a multiloci database of phylogenetic markers for Trichoderma and Hypocrea powered by sequence diagnosis and similarity search toolsMycol Res109658660CrossRefPubMedGoogle Scholar
  31. Kovacs, K, Szakacs, G, Pusztahelyi, T, Pandey, A 2004Production of chitinolytic enzymes with Trichoderma longibrachiatum IMI 92027 in solid substrate fermentationAppl Biochem Biotechnol118189204CrossRefPubMedGoogle Scholar
  32. Kraus, G, Druzhinina, I, Bissett, J, Prillinger, HJ, Szakacs, G, Koptchinski, A, Gams, W, Kubicek, CP 2004Trichoderma brevicompactum sp. novMycologia9610591073Google Scholar
  33. Kredics, L, Antal, Z, Doczi, I, Manczinger, L, Kevei, F, Nagy, E 2003Clinical importance of the genus Trichoderma. A reviewActa Microbiol Immunol Hung50105117CrossRefPubMedGoogle Scholar
  34. Kubicek, CP, Bissett, J, Druzhinina, IS, Kullnig-Gradinger, CM, Szakacs, G 2003Genetic and metabolic diversity of Trichoderma: a case study on South East Asian isolatesFungal Genet Biol38310319CrossRefPubMedGoogle Scholar
  35. Kubicek, CP, Penttilä, ME 1998

    Regulation of production of plant polysaccharide degrading enzymes by Trichoderma

    Harman, GEKubicek, CP eds. Trichoderma and Gliocladium, vol 2. Enzymes, biological control and commercial applicationsTaylor & FrancisLondon4971
    Google Scholar
  36. Kuhls, K, Lieckfeldt, E, Samuels, GJ, Kovacs, W, Meyer, W, Petrini, O, Gams, W, Börner, T, Kubicek, CP 1996Molecular evidence that the asexual industrial fungus Trichoderma reesei is a clonal derivative of the ascomycete Hypocrea jecorinaProc Natl Acad Sci USA9377557760CrossRefPubMedGoogle Scholar
  37. Kuhls, K, Lieckfeldt, E, Samuels, GJ, Meyer, W, Kubicek, CP, Börner, T 1997Revision of Trichoderma section Longibrachiatum including related teleomorphs based on an analysis of ribosomal DNA internal transcribed spacer sequencesMycologia89442460Google Scholar
  38. Kullnig, CM, Szakacs, G, Kubicek, CP 2000Molecular identification of Trichoderma species from Russia, Siberia and the HimalayaMycol Res10411171125CrossRefGoogle Scholar
  39. Kullnig-Gradinger, CM, Szakacs, G, Kubicek, CP 2002Phylogeny and evolution of the fungal genus Trichoderma: a multigene approachMycol Res106757767CrossRefGoogle Scholar
  40. Lieckfeldt, E, Kuhls, K, Muthumeenakshi, M 1998

    Molecular taxonomy of Trichoderma and Gliocladium and their teleomorphs

    Kubicek, CPHarman, GE eds. Trichoderma and Gliocladium, vol 1. Basic biology, taxonomy and geneticsTaylor & FrancisLondon3574
    Google Scholar
  41. Linnaeus C (1703) Systema naturae. Halae MagdesburgicaeGoogle Scholar
  42. Lu, B, Druzhinina, I, Fallah, P, Chaverri, P, Gradinger, C, Kubicek, CP, Samuels, GJ 2004Hypocrea/Trichoderma species with pachybasium-like conidiophores: teleomorphs for T. minutisporum and T. polysporum, and their newly discovered relativesMycologia96310342Google Scholar
  43. Lutzoni, F, Pagel, M, Reeb, V 2001Major fungal lineages are derived from lichen symbiotic ancestorsNature (Lond)411937940CrossRefGoogle Scholar
  44. Nelson, EE 1982Occurrence of Trichoderma in a Douglas-fir soilMycologia74280284Google Scholar
  45. O'Donnell, K, Cigelnik, E, Nirenberg, HI 1998Molecular systematics and phylogeography of the Gibberella fujikuroi species complexMycologia90465493Google Scholar
  46. O'Donnell, K, Nirenberg, HI, Aoki, T, Cigelnik, E 2000A multigene phylogeny of the Gibberella fujikuroi species complex: detection of additional phylogenetically distinct speciesMycoscience416178Google Scholar
  47. Penttilä, ME 1998

    Heterologous protein production in Trichoderma

    Harman, GEKubicek, CP eds. Trichoderma and Gliocladium, vol 2. Enzymes, biological control and commercial applicationsTaylor & FrancisLondon356383
    Google Scholar
  48. Persoon, CH 1794Disposita methodical fungorumRömers Neues Mag Bot181128Google Scholar
  49. Rannala, B, Yang, Z 1996Probability distribution of molecular evolutionary trees: a new method of phylogenetic interferenceJ Mol Evol43304311PubMedGoogle Scholar
  50. Rifai, MA 1969A revision of the genus TrichodermaMycol Pap116156Google Scholar
  51. Rifai, MA, Webster, J 1966aCulture studies of Hypocrea and Trichoderma II. H. aureoviridis and H. rufa f. sterilis f. novTrans Br Mycol Soc49289296CrossRefGoogle Scholar
  52. Rifai, MA, Webster, J 1966bCulture studies on Hypocrea and Trichoderma III. H. lactea (=H. citrina) and H. pulvinataTrans Br Mycol Soc49297310Google Scholar
  53. Salemi, M, Vandamme, A 2003The phylogenetic handbook. A practical approach to DNA and protein phylogenyCambridge University PressCambridgeGoogle Scholar
  54. Samuels, GJ 1996Trichoderma: a review of biology and systematics of the genusMycol Res100923935CrossRefGoogle Scholar
  55. Sivasithamparam, K, Ghisalberti, EL 1998

    Secondary metabolism in Trichoderma and Gliocladium

    Kubicek, CPHarman, GE eds. Trichoderma and Gliocladium, vol 1. Basic biology, taxonomy and geneticsTaylor & FrancisLondon139191
    Google Scholar
  56. Taylor, JW, Jacobson, DJ, Kroken, S, Kasuga, T, Geiser, DM, Hibbett, DS, Fisher, MC 2000Phylogenetic species recognition and species concepts in fungiFungal Genet Biol312132CrossRefPubMedGoogle Scholar
  57. Taylor, JW, Spatafora, J, O'Donnell, K, Lutzoni, F, James, T, Hibbett, DS, Geiser, D, Bruns, TD, Blackwell, M 2004

    The Fungi

    Cracraft, JDonoghue, MJ eds. Assembling the tree of lifeOxford University PressNew York171194
    Google Scholar
  58. Thrane, U, Poulsen, SB, Nirenberg, HI, Lieckfeldt, E 2001Identification of Trichoderma strains by image analysis of HPLC chromatogramsFEMS Microbiol Lett203249255PubMedGoogle Scholar
  59. Tulasne, L, Tulasne, R 1860De quelques Sphéries fungicoles, à propos d'un mémoire de M. Antoine de Bary sur les NyctalisAnn Sci Nat Bot13519Google Scholar
  60. Wey, TT, Hseu, TH, Huang, L 1994Molecular cloning and sequence analysis of the cellobiohydrolase I gene from Trichoderma koningii G-39Curr Microbiol283139CrossRefPubMedGoogle Scholar
  61. Widden, P, Abitbol, JJ 1980Seasonality of Trichoderma species in a spruce-forest soilMycologia72775784Google Scholar
  62. Wuczskowski, M, Druzhinina, IS, Gherbawy, Y, Klug, B, Prillinger, HJ, Kubicek, CP 2003Taxon pattern and genetic diversity of Trichoderma in a mid-European, primeval floodplain-forestMicrobiol Res158125134CrossRefGoogle Scholar
  63. Zhang, CL, Druzhinina, IS, Kubicek, CP, Xu, T 2005Biodiversity of Trichoderma in China: evidence for a North to South difference of species distribution in East AsiaFEMS Microbiol Lett251251257CrossRefPubMedGoogle Scholar

Copyright information

© The Mycological Society of Japan and Springer-Verlag Tokyo 2006

Authors and Affiliations

  • Irina S. Druzhinina
    • 1
  • Alex G. Kopchinskiy
    • 1
  • Christian P. Kubicek
    • 1
  1. 1.Research Area of Gene Technology and Applied Biochemistry, Institute of Chemical Engineering (ICE)Vienna University of TechnologyViennaAustria

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