Systematics of the Trichoderma harzianum species complex and the re-identification of commercial biocontrol strains

Literature cited

• AhmadJSBakerR. 1987a. Competitive saprophytic ability and cellulolytic activity of rhizosphere-competent mutants of Trichoderma harzianum. Phytopathology 77: 358–362.
   Web of Science ®Google Scholar
• AhmadJS. 1987b. Rhizosphere competence of Trichoderma harzianum. Phytopathology 77:182–189.
   Web of Science ®Google Scholar
• AviseJCBallRM. 1990. Principles of genealogical concordance in species concepts and biological taxonomy. Oxford Surv Evol Biol 7:45–67.
   PubMed Web of Science ®Google Scholar
• BaileyBABaeHStremMDCrozierJThomasSESamuelsGJVinyardBTHolmesKA. 2008. Antibiosis, mycoparasitism and colonization success for endophytic Trichoderma isolates with biocontrol potential in Theobroma cacao. Biol Control 46:24–35, doi:10.1016/j.biocontrol.2008.01.003
   Web of Science ®Google Scholar
• BaileyBA. 1991. A revision of the genus Trichoderma III. Section Pachybasium. Can J Bot 69:2373–2416, doi:10.1139/b91-298
   Google Scholar
• BazinetALCummingsMP. 2008. The Lattice Project: a grid research and production environment combining multiple grid computing models. In: WeberMHW, ed. Distributed & grid computing—Science made transparent for everyone. Rechenkraft.net.
   Google Scholar
• BrasierC. 2000. Plant pathology—the rise of the hybrid fungi. Nature 405:134–135, doi:10.1038/35012193
   PubMed Web of Science ®Google Scholar
• CarboneIKohnLM. 1999. A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553–556.
   Web of Science ®Google Scholar
• ChaverriPCastleburyLASamuelsGJGeiserDM. 2003. Multilocus phylogenetic structure of Trichoderma harzianum/Hypocrea lixii complex. Mol Phylogenet Evol 27:302–313, doi:10.1016/S1055-7903(02)00400-1
   Google Scholar
• ChaverriPGazisRSamuelsGJ. 2011. Trichoderma amazonicum, a new endophytic species on Hevea brasiliensis and H. guianensis from the Amazon basin. Mycologia 103:139–151, doi:10.3852/10-078
   PubMed Web of Science ®Google Scholar
• ChaverriPSamuelsGJ. 2002. Hypocrea lixii Pat., the teleomorph of Trichoderma harzianum Rifai. Mycol Prog 1: 283–286.
   Google Scholar
• ChaverriPSamuelsGJ. 2003. Hypocrea/Trichoderma (Ascomycota, Hypocreales, Hypocreaceae): species with green ascospores. Stud Mycol 48:1–116.
   Google Scholar
• ChaverriPSamuelsGJ. 2013. Evolution of habitat preference and nutrition mode in a cosmopolitan fungal genus with evidence of interkingdom host jumps and major shifts in ecology. Evolution 7:2823–2837, doi:10.1111/evo.12169
   Google Scholar
• ChowdappaPKumarSPMLakshmiMJUpretiKK. 2013. Growth stimulation and induction of systemic resistance in tomato against early and late blight by Bacillus subtilis OTPB1 or Trichoderma harzianum OTPB3. Biol Control 65:109–117, doi:10.1016/j.biocontrol.2012.11.009
   Web of Science ®Google Scholar
• CummingsMPHuskampJC. 2005. Grid computing. Educause Rev 40:116–117.
   Google Scholar
• DegenkolbTDieckmannRNielsenKFGräfenhanTTheisCZafariDChaverriPIsmaielABrücknerHvon DöhrenHSamuelsGJ. 2008. The Trichoderma brevicompactum clade: a separate lineage with new species, new peptaibiotics and mycotoxins. Mycol Prog 7:177–219, doi:10.1007/s11557-008-0563-3
   Google Scholar
• DegenkolbTNielsenKFDieckmannRBranco-RochaFChaverriPSamuelsGJThraneUvon DöhrenHVilcinskasABrücknerH. 2015. Peptaibol, secondary metabolite, and hydrophobin pattern of commercial biocontrol agents formulated with species of the Trichoderma harzianum complex. Chem Biodivers 12:662–684, doi:10.1002/cbdv.201400300
   Google Scholar
• DettmanJRJacobsonDJTaylorJW. 2003. A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution 57:2703–2720.
   PubMed Web of Science ®Google Scholar
• DruzhininaISKomoń-ZelazowskaMAtanasovaLSeidlVKubicekCP. 2010a. Evolution and ecophysiology of the industrial producer Hypocrea jecorina (Anamorph Trichoderma reesei) and a new sympatric agamospecies related to it. PLos ONE 5:e9191, doi:10.1371/journal.pone0009191
   Google Scholar
• DruzhininaISKubicekCPKomoń-ZelazowskaMMulawTBBissettJ. 2010b. The Trichoderma harzianum demon: complex speciation history resulting in coexistence of hypothetical biological species, recent agamospecies and numerous relict lineages. BMC Evol Biol 10:94–107, doi:10.1186/1471-2148-10-94
   PubMed Web of Science ®Google Scholar
• DruzhininaISSeidl-SeibothVHerrera-EstrellaAHorwitzBAKenerleyCMMonteEMukherjeePKZeilingerSGrigorievIVKubicekCP. 2011. Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9:749–759, doi:10.1038/nrmicro2637
   PubMed Web of Science ®Google Scholar
• EvansHCHolmesKAThomasSE. 2003. Endophytes and mycoparasites associated with an indigenous forest tree, Theobroma gileri, in Ecuador and a preliminary assessment of their potential as biocontrol agents of cocoa diseases. Mycol Prog 2:149–160.
   Google Scholar
• FravelDR. 2005. Commercialization and implementation of biocontrol. Annu Rev Phytopathol 43:337–359.
   PubMed Web of Science ®Google Scholar
• Funck-JensenDLumsdenRD. 1999. Biological control of soilborne pathogens. In: AlbajesRGullinoLvan LenterenJCEladY, eds. Integrated pest and disease management in greenhouse crops. Dordrecht, the Netherlands: NL. Kluwer Academic Publishers. p 319–332.
   Google Scholar
• GamsWMeyerW. 1998. What exactly is Trichoderma harzianum? Mycologia, 90:904–915.
   Web of Science ®Google Scholar
• GazisRChaverriP. 2010. Diversity of fungal endophytes in leaves and stems of rubber trees (Hevea brasiliensis) in Tambopata, Peru. Fungal Ecol 3:240–254, doi:10.1016/j.funeco.2009.12.001
   Web of Science ®Google Scholar
• GazisRRehnerSChaverriP. 2011. Species delimitation in fungal endophyte diversity studies and its implications in ecological and biogeographic inferences. Mol Ecol 20:3001–3013, doi:10.1111/j.1365-294X.2011.05110.x
   PubMed Web of Science ®Google Scholar
• GrondonaIHermosaMRTejadaMGomisMDMateosPFBridgePDMonteEGarcía-AchaI. 1997. Physiological and biochemical characterization of Trichoderma harzianum, a biological control agent against soilborne fungal plant pathogens. Appl Environ Microbiol 63:3189–3198.
   PubMed Web of Science ®Google Scholar
• HarmanGE. 2000. Myths and dogmas of biocontrol. Changes in perceptions derived from research on Trichoderma harzianum T-22. Plant Dis 84:377–393.
   PubMed Web of Science ®Google Scholar
• HarmanGEHowellCRViterboAChetILoritoM. 2004. Trichoderma species—Opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56, doi:10.1038/nrmicro797
   PubMed Web of Science ®Google Scholar
• HarmanGEKubicekCP, eds. 1998. Trichoderma and Gliocladium. Vol. 2. Enzymes, biological control and commercial applications. London: Taylor & Francis. xiv + 393 p.
   Google Scholar
• HirookaYRossmanAYChaverriP. 2011. Morphological and phylogenetic analyses of the Nectria cinnabarina species complex. Stud Mycol 68:35–56.
   PubMed Web of Science ®Google Scholar
• Hoyos-CarvajalLOrduzSBissettJ. 2009. Genetic and metabolic biodiversity of Trichoderma from Colombia and adjacent neotropic regions. Fungal Genet Biol 46:615–631, doi:10.1016/j.fgb.2009.04.006
   PubMed Web of Science ®Google Scholar
• HuelsenbeckJPRonquistFNielsenESBollbackJP. 2001. Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294:2310–2314, doi:10.1126/science.1065889
   PubMed Web of Science ®Google Scholar
• IidaASanekataMFujitaTTanakaHEnokiAFuseGKanaiMRudewiczPJTachikawaE. 1994. Fungal metabolites XVI. Structures of new peptaibols, tricho-kindins I–VII, from the fungus Trichoderma harzianum. Chem Pharm Bull (Tokyo) 42:1070–1075.
   Google Scholar
• JaklitschWM. 2009. European species of Hypocrea I. The green-spored species. Stud Mycol 63:1–91.
   PubMedGoogle Scholar
• JaklitschWM. 2011. European species of Hypocrea II. Fungal Divers 48:1–250, 10 p, doi:10.1007/s13225-011-0088-y
   Web of Science ®Google Scholar
• KaewchaiSSoytongKHydeKD. 2009. Mycofungicides and fungal biofertilizers. Fungal Divers 38:25–50.
   Web of Science ®Google Scholar
• KatohKKumaK-iTohHMiyataT. 2005. MAFFT 5: improvement in accuracy of multiple sequence alignment Nucleic Acids Res 33:511–518, doi:10.1093/nar/gki198
   PubMed Web of Science ®Google Scholar
• KowalskiTKehrRD. 1996. Fungal endophytes in living branch bases in several European tree species. In: RedlinSCCarrisLM, eds. Endophytic fungi in grasses and woody plants: systematics, ecology and evolution. St. Paul, Minnesota: APS Press. p 67–86.
   Google Scholar
• KubicekCPHerrera-EstrellaASeidl-SeibothVMartinezDADruzhininaISThonMZeilingerSCasas-FloresSHorwitzBAMukherjeePKMukherjeeMKredicsLAlcarazLDAertsAAntalZAtanasovaLCervantes-BadilloMGChallacombeJChertkovOMcCluskeyKCoulpierFDeshpandeNDoehrenHvEbboleDJEsquivel-NaranjoEUFeketeEFlipphiMGlaserFGomez-RodriguezEYGruberSHanCHenrissatBHermosaRHernandez-OnateMKaraffaLKostiICromSLLindquistELucasSLubeckMLubeckPSMargeotAMetzBMisraMNevalainenHOmannMPackerNPerroneGUresti-RiveraEESalamovASchmollMSeibothBShapiroHSuknoSTamayo-RamosJATischDWiestAWilkinsonHHZhangMCoutinhoPMKenerleyCMMonteEBakerSEGrigorievIV. 2011. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol 12:R40, doi:10.1186/gb-2011-12-4-r40
   PubMed Web of Science ®Google Scholar
• KullnigCMKrupicaTWooSLMachRLReyMLoritoMKubicekCP. 2001. Confusion abounds over identities of Trichoderma biocontrol isolates. Mycol Res 105:770–772, doi:10.1017/S0953756201229967
   Google Scholar
• LiQ-RTanPJiangY-LHydeKDMcKenzieEHCBahkaliAHKangJ-CWangY. 2012. A novel Trichoderma species isolated from soil in Guizhou, T. guizhouense. Mycol Prog 12:167–172.
   Google Scholar
• LiuKRaghavanSNelesenSLinderCRWarnowT. 2009. Rapid and accurate large-scale coestimation of sequence alignments and phylogenetic trees. Science 324:1561–1564, doi:10.1126/science.1171243
   PubMed Web of Science ®Google Scholar
• LiuYJWhelenSHallBD. 1999. Phylogenetic relationships among Ascomycetes: evidence from an RNA polymerase II subunit. Mol Biol Evol 16:1799–1808.
   PubMed Web of Science ®Google Scholar
• LoCTNelsonEBHarmanGE. 1997. Improved biocontrol efficacy of Trichoderma harzianum 1295-22 for foliar phases of turf diseases by use of spray applications. Plant Dis 81:1132–1138.
   Google Scholar
• MaddisonWPMaddisonDR. 2009. Mesquite 2.5: a modular system for evolutionary analysis. http://mesquiteproject.org.
   Google Scholar
• Mason-GamerRJKelloggEA. 1996. Testing for phylogenetic conflict among molecular datasets in the tribe Triticeae (Gramineae). Syst Biol 45:524–545.
   Web of Science ®Google Scholar
• MyersDSBazinetALCummingsMP. 2008. Expanding the reach of Grid computing: combining Globus- and BOINC-based systems. In: TalbiE-GZomayaA, eds. Grids for bioinformatics and computational biology. New York: John Wiley & Sons. p 71–85.
   Google Scholar
• NirenbergHI. 1976. Untersuchungen über die morphologische und biologische Differenzierung in der Fusarium-Sektion Liseola. Mitt Biol Bundesanst Land-Forstw Berlin-Dahlem 169:1–117.
   Google Scholar
• PanSLiuLFuX-SZhengW-JWangW-M. 2012. High Throughput screening and detection of peptaibol antibiotics from the fermentation broth of Trichoderma harzianum by LC-MS/MS. Chin Pharm J 47:1849–1855.
   Google Scholar
• ParkMSBaeKSYuSH. 2006. Two new species of Trichoderma associated with green mold epidemic of oyster mushroom cultivation in Korea. Mycobiology 34:111–113, doi:10.4489/MYCO.2006.34.3.111
   Google Scholar
• PaulitzTCBelangerRR. 2001. Biological control in greenhouse systems. Annu Rev Phytopathol 39:103–133, doi:10.1146/annurev.phyto.39.1.103
   PubMed Web of Science ®Google Scholar
• PosadaD. 2008. jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256, doi:10.1093/molbev/msn083
   PubMed Web of Science ®Google Scholar
• RambautADrummondAJ. 2007. Tracer 1.4. Available from http://beast.bio.ed.ac.uk/Tracer.
   Google Scholar
• ReebVLutzoniFRouxC. 2004. Contribution of RPB2 to multilocus phylogenetic studies of the euascomycetes (Pezizomycotina, Fungi) with special emphasis on lichen-forming Acarosporaceae and evolution of polyspory. Mol Phylogenet Evol 32:1036–1060, doi:10.1016/j.ympev.2004.04.012
   PubMed Web of Science ®Google Scholar
• RehnerSA. 2001. Primers for elongation factor 1-alpha (EF1-alpha). Available from www.aftol.org/pdfs/EF1primer.pdf.
   Google Scholar
• RifaiMA. 1969. A revision of the genus Trichoderma. Mycol Pap 116:1–56.
   Google Scholar
• RojasEIRehnerSASamuelsGJvan BaelSAHerreEACannonPChenRPangJFWangRWZhangYPPengYQShaT. 2010. Colletotrichum gloeosporioides s.l. associated with Theobroma cacao and other plants in Panama: multilocus phylogenies distinguish host-associated pathogens from asymptomatic endophytes. Mycologia 102:1318–1338, doi:10.3852/09-244
   PubMed Web of Science ®Google Scholar
• RonquistF. 2004. Bayesian inference of character evolution. Trends Ecol Evol 19:475–481, doi:10.1016/j.tree.2004.07.002
   PubMed Web of Science ®Google Scholar
• SalgadoCRossmanAYSamuelsGJCapdetMChaverriP. 2012. Multigene phylogenetic analyses of the Thelonectria coronata and T. veuillotiana species complexes. Mycologia 104:1325–1350, doi:10.3852/12-055
   Google Scholar
• SamuelsGJ. 1996. Trichoderma: a review of biology and systematics of the genus. Mycol Res 100:923–935.
   Web of Science ®Google Scholar
• SamuelsGJ. 2006. Trichoderma: systematics, the sexual state and ecology. Phytopathology 96:195–206, doi:10.1094/PHYTO-96-0195
   PubMed Web of Science ®Google Scholar
• SamuelsGJDoddSLGamsWCastleburyLAPetriniO. 2002. Trichoderma species associated with the green mold epidemic of commercially grown Agaricus bisporus. Mycologia 94:146–168.
   PubMed Web of Science ®Google Scholar
• SamuelsGJDoiYRogersonCT. 1990. Hypocreales. In: Contributions toward a mycobiota of Indonesia. SamuelsGJ, ed. Mem NY Bot Gard 59:6–108.
   Google Scholar
• SamuelsGJHebbarPK. 2015. The Trichoderma manual. Their identification and application in agriculture. St Paul, Minnesota: APS Press (in press).
   Google Scholar
• SamuelsGJIsmaielA. 2009. Trichoderma evansii and T. lieckfeldtiae: two new T. hamatum-like species. Mycologia 101:142–156, doi:10.3852/08-161
   PubMed Web of Science ®Google Scholar
• Sandoval-DenisMSuttonDACano-LiraJFGenéJFothergillAWWiederholdNGuarroJ. 2014. Phylogeny of the clinically relevant species of the emerging fungus Trichoderma and their antifungal susceptibilities. J Clin Microbiol 52: 2112–2125, doi:10.1128/JCM.00429-14
   PubMed Web of Science ®Google Scholar
• SangTZhongY. 2000. Testing hybridization hypotheses based on incongruent gene trees. Syst Biol 49:422–434.
   Web of Science ®Google Scholar
• SavoieJMIapiccoRLargeteau-MamounML. 2001. Factors influencing the competitive saprophytic ability of Trichoderma harzianum Th2 in mushroom (Agaricus bisporus) compost. Mycol Res 105:1348–1356, doi:10.1017/S0953756201004993
   Google Scholar
• SchochCLSeifertKAHuhndorfSRobertVSpougeJLLevesqueAChenWConsortiumFB. 2012. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci (USA) 109:6241–6246, doi:10.1073/pnas.1117018109
   PubMed Web of Science ®Google Scholar
• SchroersHJO’DonnellKLamprechtSCKammeyerPLJohnsonSSuttonDARinaldiMGGeiserDMSummerbellRC. 2009. Taxonomy and phylogeny of the Fusarium dimerum species group. Mycologia 101:44–70, doi:10.3852/08-00
   Web of Science ®Google Scholar
• SeifertKARossmanAY. 2010. How to describe a new fungal species. IMA Fungus 1:109–116.
   Google Scholar
• SharmaRRSinghDSinghR. 2009. Biological control of postharvest diseases of fruits and vegetables by microbial antagonists: a review. Biol Control 50:205–221, doi:10.1016/j.biocontrol.2009.05.001
   Web of Science ®Google Scholar
• SharonEChetIViterboABar-EyalMNaganHSamuelsGJSpiegelY. 2007. Parasitism of Trichoderma on Meloidogyne javanica and role of the gelatinous matrix. Eur J Plant Pathol 118:247–258, 10 p, doi:10.1007/s10658-007-9140-x
   Web of Science ®Google Scholar
• StamatakisA. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690, doi:10.1093/bioinformatics/btl446
   PubMed Web of Science ®Google Scholar
• StaszTEHarmanGEWeedenNF. 1988. Protoplast preparation and fusion in two biocontrol strains of Trichoderma harzianum. Mycologia 80:141–150.
   Web of Science ®Google Scholar
• TamuraKPetersonDPetersonNStecherGNeiMKumarS. 2011. MEGA 5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Mol Biol Evol 28:2731–2739, doi:10.1093/molbev/msr121
   PubMed Web of Science ®Google Scholar
• VeerkampJGamsW. 1983. Los hongos de Colombia VIII. Some new species of soil fungi from Colombia. Caldasia 13:709–717.
   Google Scholar
• WagnerCEKellerIWittwerSSelzOMMwaikoSGreuterLSivasundarASeehausenO. 2013. Genomewide RAD sequence data provide unprecedented resolution of species boundaries and relationships in the Lake Victoria cichlid adaptive radiation. Mol Ecol 22:787–798, doi:10.1111/mec.12023
   PubMed Web of Science ®Google Scholar
• WhiteTJBrunsTLeeSTaylorJW. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: InnisMAGelfandDHSninskyJJWhiteTJ, eds. PCR protocols: a guide to methods and applications. New York: Academic Press. p 315–322.
   Google Scholar
• ZwicklDJ. 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion [doctoral dissertation]. Austin: Univ. Texas Press. 115 p.
   Google Scholar