Skip to main content
Log in

Species concepts and biodiversity in Trichoderma and Hypocrea: from aggregate species to species clusters?

  • Articles
  • Published:
Journal of Zhejiang University-SCIENCE B Aims and scope Submit manuscript

Abstract

Trichoderma/Hypocrea is a genus of soil-borne or wood-decaying fungi containing members important to mankind as producers of industrial enzymes and biocontrol agents against plant pathogens, but also as opportunistic pathogens of immunocompromised humans. Species identification, while essential in view of the controversial properties of taxa of this genus, has been problematic by traditional methods. Here we will present a critical survey of the various identification methods in use. In addition, we will present an update on the taxonomy and phylogeny of the 88 taxa (which occur as 14 holomorphs 49 teleomorphs and 25 anamorphs in nature) of Trichoderma/Hypocrea that have been confirmed by a combination of morphological, physiological and genetic approaches.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bisby, G.R., 1939.Trichoderma viride Pers. ex Fries, and notes onHypocrea.Trans Brit Mycol Soc,23:149–168.

    Article  Google Scholar 

  • Bissett, J., 1984. A revision of the genusTrichoderma. I. Sect.Longibrachiatum sect. nov.Can J Bot,62:924–931.

    Article  Google Scholar 

  • Bissett, J., 1991a. A revision of the genusTrichoderma. II. Infrageneric classification.Can J Bot,69:2357–2372.

    Article  Google Scholar 

  • Bissett, J., 1991b. A revision of the genusTrichoderma. III. Sect.Pachybasium. Can J Bot,69:2373–2417.

    Article  Google Scholar 

  • Bissett, J., 1991c. A revision of the genusTrichoderma. IV. Additional notes on sectionLongibrachiatum.Can J Bot,69:2418–2420.

    Article  Google Scholar 

  • Bissett, J., 1992.Trichoderma atroviride.Can J Bot,70:639–641.

    Article  Google Scholar 

  • Bissett, J., Szakacs, G., Nolan, C.A., Druzhinina, I., Kullnig-Gradinger, C.M., Kubicek, C.P., 2003. Seven new taxa ofTrichoderma from Asia.Can J Bot,81:570–586.

    Article  Google Scholar 

  • Buckler, E.S., Ippolito, A., Holtsfort, T.E., 1997. The evolution of ribosomal DNA: divergent paralogues and phylogenetic implications.Genetics,145:821–832.

    Article  CAS  PubMed  Google Scholar 

  • Chaverri, P., Castlebury, L.A., Samuels, G.J., Geiser, D., 2003a. Multilocus phylogenetic structure within theTrichoderma harzianum/Hypocrea lixii complex.Mol. Phylogenet. Evol.,27:302–313.

    Article  CAS  PubMed  Google Scholar 

  • Chaverri, P., Castlebury, L.A., Overton, B.E., Samuels, G.J., 2003b.Hypocreal/Trichoderma: species with conidiophore elongations and green conidia.Mycologia,95:1100–1140.

    Article  PubMed  Google Scholar 

  • Chaverri, P., Candoussau, F., Samuels, G.J., 2004.Hypocrea phyllostachydis and itsTrichoderma anamorph, a new bambusicolous species from France.Mycol Progr,3:29–36.

    Article  Google Scholar 

  • Dodd, S.L., Crowhurst, R.N., Rodrigo, A.C., Samuels, G.J., Hill, R.A., Stewart, A., 2000. Examination ofTrichoderma phylogenies derived from ribosomal DNA sequence data.Mycol Res,104:23–34.

    Article  CAS  Google Scholar 

  • Dodd, S.L., Lieckfeldt, E., Chaverri, P., Overton B.E., Samuels, G.J., 2002. Taxonomy and phylogenetic relationships of two species ofHypocrea withTrichoderma anamorphs.Mycol Progr,1:409–428.

    Article  Google Scholar 

  • Dodd, S.L., Lieckfeldt, E., Samuels, G.J., 2003.Hypocrea atroviridis sp. nov. the teleomorph ofTrichoderma atroviride.Mycologia,95:27–40.

    Article  PubMed  Google Scholar 

  • Doi, Y., 1972. Revision of theHypocreales with cultural observations. IV. The genusHypocrea and its allies in Japan. (2) Enumeration of the species.Bull Natl Sci Museum Tokyo,15:649–751.

    Google Scholar 

  • Doi, Y., Abe, Y., Sugyama, J., 1987.Trichoderma sect.Saturnisporum, sect. nov. andTrichoderma ghanense, sp. nov.Bull Nat Sci Museum, Ser B (Botany),12:1–9.

    Google Scholar 

  • Druzhinina, I., Chaverri, P., Fallah, P., Kubicek, C.P., Samuels, G.J., 2004a.Hypocrea flavoconidia, a new species with yellow conidia from Costa Rica.Stud Mycol, in press.

  • Druzhinina, I., Koptchinski, A., Komon, M., Bissett, J., Szakacs, G., Kubicek, C.P., 2004b. A DNA-barcode for strain identification inTrichoderma. Manuscript submitted.

  • Gams, W., Bissett, J., 1998. Morphology and Identification ofTrichoderma.In: Kubicek, C.P., Harman, G.E. (Eds.),Trichoderma andGliocladium. Vol. 1. Basic Biology, Taxonomy and Genetics. Taylor and Francis Ltd., London, p.3–34.

    Google Scholar 

  • Gherbawy, Y., Druzhinina, I., Shaban, G.M., Wuczkowsky, M., Yaser, M., El-Naghy, M.A., Prillinger, H.J., Kubicek, C.P., 2004.Trichoderma populations from alkaline agricultural soil in the Nile valley, Egypt, consist of only two species.Mycol Prog,3:211–218.

    Article  Google Scholar 

  • Hermosa, M.R., Grondona, I., Iturriaga, E.A., Diaz-Minguez, J.M., Castro, C., Monte, E., Garcia-Acha, I., 2000. Molecular characterization and identification of biocontrol isolates ofTrichoderma spp.Appl Environ Microbiol,66:1890–1898.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hermosa, M.R., Keck, E., Chamorro, I., Rubio, B., Sanz, L., Vizcaino, J.A., Grondona, I., Monte, E., 2004. Genetic diversity shown inTrichoderma biocontrol isolates.Mycol Res,108:897–906.

    Article  CAS  PubMed  Google Scholar 

  • Hjeljord, L., Tronsmo, A., 1998.Trichoderma andGliocladium in Biological Control: An Overview.In: Harman, G.E., Kubicek, C.P. (Eds.),Trichoderma andGliocladium. Vol. 2. Enzymes, Biological Control and Commercial Applications. Taylor and Francis Ltd., London, p.131–151.

    Google Scholar 

  • Huelsenbeck, J.P., Ronquist, F., 2001. MRBAYES: Bayesian inference of phylogenetic trees.Bioinformatics,17:754–755.

    Article  CAS  PubMed  Google Scholar 

  • Kindermann, J., El-Ayouti, Y., Samuels, G.J., Kubicek, C.P., 1998. Phylogeny of the genusTrichoderma based on sequence analysis of the internal transcribed spacer region 1 of the rDNA clade.Fungal Genet Biol,24:298–309.

    Article  CAS  PubMed  Google Scholar 

  • Klein, D., Eveleigh, D.E., 1998. Ecology ofTrichoderma.In: Kubicek, C.P., Harman, G.E. (Eds.),Trichoderma andGliocladium. Vol. 1. Basic Biology, Taxonomy and Genetics. Taylor and Francis Ltd., London, p.57–74.

    Google Scholar 

  • Kraus, G., Druzhinina, I., Bissett, J., Zafari, D., Prillinger, H.J., Szakacs, G., Zare, R., Gams, W., Kubicek, C.P., 2004.Trichoderma brevicompactum sp. nov.Mycologia,96:1057–1071.

    Article  Google Scholar 

  • Kredics, L., Antal, Z., Doczi, I., Manczinger, L., Kevei, F., Nagy, E., 2003. Clinical importance of the genusTrichoderma. A review.Acta Microbiol Immunol Hung,50:105–17.

    Article  CAS  PubMed  Google Scholar 

  • Kubicek, C.P., Penttilä, M.E., 1998. Regulation of Production of Plant Polysaccharide Degrading Enzymes byTrichoderma.In: Harman, G.E., Kubicek, C.P. (Eds.),Trichoderma andGliocladium. Vol. 2. Enzymes, Biological Control and Commercial Applications. Taylor and Francis Ltd., London, p.49–71.

    Google Scholar 

  • Kubicek, C.P., Bissett, J., Druzhinina, I., Kullnig-Gradinger, C.M., Szakacs, G., 2003. Genetic and metabolic diversity ofTrichoderma: a case study on South East Asian isolates.Fungal Genet Biol,38:310–319.

    Article  CAS  PubMed  Google Scholar 

  • Kuhls, K., Lieckfeldt, E., Samuels, G.J., Kovacs, W., Meyer, W., Petrini, O., Gams, W., Börner, T., Kubicek, C.P., 1996. Molecular evidence that the asexual industrial fungusTrichoderma reesei is a clonal derivative of the ascomyceteHypocrea jecorina.Proc. Natl Acad Sci USA,93:7755–7760.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuhls, K., Lieckfeldt, E., Samuels, G.J., Meyer, W., Kubicek, C.P., Börner, T., 1997. Revision ofTrichoderma sectionLongibrachiatum including related teleomorphs based on an analysis of ribosomal DNA internal transcribed spacer sequences.Mycologia,89:442–460.

    Article  CAS  Google Scholar 

  • Kullnig, C.M., Szakacs, G., Kubicek, C.P., 2000. Molecular identification ofTrichoderma species from Russia, Siberia and the Himalaya.Mycol Res,104:1117–1125.

    Article  CAS  Google Scholar 

  • Kullnig, C.M., Krupica, T., Woo, S.L., Mach, R.L., Rey, M., Benitez, T., Lorito, M., Kubicek, C.P., 2001. Confusion abounds over identity ofTrichoderma biocontrol isolates.Mycol Res,105:769–772.

    Article  Google Scholar 

  • Kullnig-Gradinger, C.M., Szakacs, G., Kubicek, C.P., 2002. Phylogeny and evolution of the fungal genusTrichoderma —a multigene approach.Mycol Res,106:757–767.

    Article  CAS  Google Scholar 

  • Lewis, P.O., 2001. Phylogenetic systematics turns over a new leaf.Trends Ecol Evol,16:30–37.

    Article  CAS  PubMed  Google Scholar 

  • Lieckfeldt, E., Seifert, K.A., 2000. An evaluation of the use of ITS sequences in the taxonomy of theHypocreales.Stud Mycol,45:35–44.

    Google Scholar 

  • Lieckfeldt, E., Samuels, G.J., Börner, T., Gams, W., 1998.Trichoderma koningii: neotypification andHypocrea teleomorph.Can J Bot,76:1507–1522.

    Google Scholar 

  • Lieckfeldt, E., Samuels, G.J., Nirenberg, H.I., Petrini, O., 1999. A morphological and molecular perspective ofTrichoderma viride: is it one or two species.Appl Environ Microbiol,65:2418–2428.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lieckfeldt, E., Kullnig, C.M., Kubicek, C.P., Samuels, G.J., Börner, T., 2001.Trichoderma aureoviride: phylogenetic position and characterization.Mycol Res,105:313–322.

    Article  CAS  Google Scholar 

  • Lu, B.S., Samuels, G.J., 2004.Hypocrea stilbohypoxyli and itsTrichoderma koningii-like anamorph from Puerto Rico onStilbohypoxylon Muelleri,Sydowia, manuscript submitted.

  • Lu, B.S., Druzhinina, I., Chaverri, P., Fallah, P., Gradinger, C., Kubicek, C.P., Samuels, G.J., 2004.Hypocreal/Trichoderma species with pachybasium-like conidiophores: teleomorphs forT. minutisporum andT. polysporum, and their newly discovered relatives.Mycologia,96:310–342.

    Article  PubMed  Google Scholar 

  • Lutzoni, F., Pagel, M., Reeb, V., 2001. Major fungal lineages are derived from lichen symbiotic ancestors.Nature,411:937–940.

    Article  CAS  PubMed  Google Scholar 

  • Metropolis, N., Rosenbluth, A.W., Rosenbluth, M.N., Teller, A.H., Teller, E., 1953. Equations of state calculations for fast computing machines.J Chem Phys,21:1087–1091.

    Article  CAS  Google Scholar 

  • Nelson, E.E., 1982. Occurrence ofTrichoderma in a Douglas-fir soil.Mycologia,74:280–284.

    Article  Google Scholar 

  • O'Donnell, K., 1992. Ribosomal DNA internal transcribed spacers are highly divergent in the phytopathogenic ascomyceteFusarium sambucinum (Gibberella pulicaris).Curr Genet,22:213–220.

    Article  CAS  PubMed  Google Scholar 

  • O'Donnell, K., Cigelnik, E., Nirenberg, H.I., 1998. Molecular systematics and phylogeography of theGibberella fujikuroi species complex.Mycologia,90:465–493.

    Article  CAS  Google Scholar 

  • Persoon, C.H., 1794. Disposito Methodica Fungorum in Classes, Ordines, Familias et Genera.In: Römer, J.J. (Ed.), Neues Magazin für Botanik. Ziegler und Söhne, Zürich, p.63–128.

    Google Scholar 

  • Rannala, B., Yang, Z., 1996. Probability distribution of molecular evolutionary trees: a new method of phylogenetic interference.J Mol Evol,43:304–311.

    Article  CAS  PubMed  Google Scholar 

  • Rifai, M.A., 1969. A revision of the genusTrichoderma.Mycol Pap,116:1–116.

    Google Scholar 

  • Salemi, M., Vandamme, A., 2003. The Phylogenetic Handbook. A Practical Approach to DNA and Protein Phylogeny. Cambidge University Press, UK.

    Google Scholar 

  • Samuels, G.J., 1996.Trichoderma: A review of biology and systematics of the genus.Mycol Res,100:923–935.

    Article  Google Scholar 

  • Samuels, G.J., 2004.Trichoderma ovalisporum: A new endophytic species with potential to control frosty pod rot of cocoa.Mycol. Prog., in press.

  • Samuels, G.J., Petrini, O., Kuhls, K., Lieckfeldt, E., Kubicek, C.P., 1998. TheHypocrea schweinitzii complex andTrichoderma sect.Longibrachiatum. Stud Mycol,41:1–54.

    Google Scholar 

  • Samuels, G.J., Dodd, S.L., Gams, W., Castlebury, L.A., Petrini, O., 2002.Trichoderma species associated with the green mold epidemic of commercially grownAgaricus bisporus.Mycologia,94:146–170.

    Article  PubMed  Google Scholar 

  • Sivasithamparam, K., Ghisalberti, E.L., 1998. Secondary Metabolism inTrichoderma andGliocladium.In: Kubicek, C.P., Harman, G.E. (Eds.),Trichoderma andGliocladium. Vol. 1. Basic Biology, Taxonomy and Genetics. Taylor and Francis Ltd., London, p.139–191.

    Google Scholar 

  • Taylor, J.W., Jacobson, D.J., Fisher, M., 1999. The evolution of asexual fungi: speciation and classification.Annu Rev Phytopathol,37:197–246.

    Article  CAS  PubMed  Google Scholar 

  • Taylor, J.W., Jacobson, D.J., Kroken, S., Kasuga, T., Geiser, D.M., Hibbett, D.S., Fisher, M.C., 2000. Phylogenetic species recognition and species concepts in fungi.Fungal Genet Biol,31:21–32.

    Article  CAS  PubMed  Google Scholar 

  • Thrane, U., Poulsen, S.B., Nirenberg, H.I., Lieckfeldt, E., 2001. Identification ofTrichoderma strains by image analysis of HPLC chromatograms.FEMS Microbiol Lett,203:249–255.

    Article  CAS  PubMed  Google Scholar 

  • Turner, D., Kovacs, W., Kuhls, K., Lieckfeldt, E., Peter, B., Arisan-Atac, I., Strauss, J., Samuels, G.J., Börner, T., Kubicek, C.P., 1997. Biogeography and phenotypic variation inTrichoderma sect.Longibrachiatum and associatedHypocrea species.Mycol Res,101:449–459.

    Article  CAS  Google Scholar 

  • Widden, P., Abitbol, J.J., 1980. Seasonality ofTrichoderma species in a spruce-forest soil.Mycologia,72:775–784.

    Article  Google Scholar 

  • Wuczskowski, M., Druzhinina, I., Gherbawy, Y., Klug, B., Prillinger, H.J., Kubicek, C.P., 2003. Taxon pattern and genetic diversity ofTrichoderma in a mid-European, primeval floodplain-forest.Microbiol Res,158:125–134.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christian P. Kubicek.

Additional information

Project supported by FWF-grants P-12748-MOB and P-16601 to C.P.K., Austria

Rights and permissions

Reprints and permissions

About this article

Cite this article

Druzhinina, I., Kubicek, C. Species concepts and biodiversity in Trichoderma and Hypocrea: from aggregate species to species clusters?. J Zheijang Univ Sci B 6, 100–112 (2005). https://doi.org/10.1631/jzus.2005.B0100

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1631/jzus.2005.B0100

Key words

CLC number

Navigation