Evolution and comparative genomics of the most common Trichoderma species

Kubicek, Christian P.; Steindorff, Andrei S.; Chenthamara, Komal; Manganiello, Gelsomina; Henrissat, Bernard; Zhang, Jian; Cai, Feng; Kopchinskiy, Alexey G.; Kubicek, Eva M.; Kuo, Alan; Baroncelli, Riccardo; Sarrocco, Sabrina; Noronha, Eliane Ferreira; Vannacci, Giovanni; Shen, Qirong; Grigoriev, Igor V.; Druzhinina, Irina S.

doi:10.1186/s12864-019-5680-7

Title: Evolution and comparative genomics of the most common Trichoderma species

Journal Article · Wed Jun 12 00:00:00 EDT 2019 · BMC Genomics

DOI:https://doi.org/10.1186/s12864-019-5680-7· OSTI ID:1619122

Kubicek, Christian P. ^[1]; Steindorff, Andrei S. ^[2]; Chenthamara, Komal ^[1]; Manganiello, Gelsomina ^[3]; Henrissat, Bernard ^[4]; Zhang, Jian ^[5]; Cai, Feng ^[5]; Kopchinskiy, Alexey G. ^[1]; Kubicek, Eva M. ^[6]; Kuo, Alan ^[7]; Baroncelli, Riccardo ^[8]; Sarrocco, Sabrina ^[9]; Noronha, Eliane Ferreira ^[10]; Vannacci, Giovanni ^[8]; Shen, Qirong ^[5]; Grigoriev, Igor V. ^[7];

^[5]

Technische Univ. Wien, Vienna (Austria). Institute of Chemical, Environmental & Bioscience Engineering (ICEBE)
Universidade de Brasília, Brasíla, DF (Brazil); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. degli Studi di Napoli Federico II, Naples, Portici (Italy)
Aix-Marseille Univ., Marseille (France); National Centre for Scientific Research (CNRS), Marseilles (France); INRA, Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
Nanjing Agricultural University, Nanjing (China). Jiangsu Provincial Key Lab of Organic Solid Waste Utilization
Vienna (Austria)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Universidad de Salamanca, Villamayor (Spain). Centro Hispano-Luso de Investigaciones Agrarias (CIALE)
Univ. of Pisa (Italy)
Universidade de Brasília, Brasíla, DF (Brazil)

Background: The growing importance of the ubiquitous fungal genus Trichoderma (Hypocreales, Ascomycota) requires understanding of its biology and evolution. Many Trichoderma species are used as biofertilizers and biofungicides and T. reesei is the model organism for industrial production of cellulolytic enzymes. In addition, some highly opportunistic species devastate mushroom farms and can become pathogens of humans. A comparative analysis of the first three whole genomes revealed mycoparasitism as the innate feature of Trichoderma. However, the evolution of these traits is not yet understood. Results: We selected 12 most commonly occurring Trichoderma species and studied the evolution of their genome sequences. Trichoderma evolved in the time of the Cretaceous-Palaeogene extinction event 66 (±15) mya, but the formation of extant sections (Longibrachiatum, Trichoderma) or clades (Harzianum/Virens) happened in Oligocene. The evolution of the Harzianum clade and section Trichoderma was accompanied by significant gene gain, but the ancestor of section Longibrachiatum experienced rapid gene loss. The highest number of genes gained encoded ankyrins, HET domain proteins and transcription factors. We also identified the Trichoderma core genome, completely curated its annotation, investigated several gene families in detail and compared the results to those of other fungi. Eighty percent of those genes for which a function could be predicted were also found in other fungi, but only 67% of those without a predictable function. Conclusions: Our study presents a time scaled pattern of genome evolution in 12 Trichoderma species from three phylogenetically distant clades/sections and a comprehensive analysis of their genes. The data offer insights in the evolution of a mycoparasite towards a generalist.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Key Research and Development Program of China; Austrian Science Foundation; CAPES foundation; CNPq; IDEX Aix Marseille

Grant/Contract Number:: AC02-05CH11231; Microbio-E, 2015–2017; P25613-B20; I-1249

OSTI ID:: 1619122

Journal Information:: BMC Genomics, Vol. 20, Issue 1; ISSN 1471-2164

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 114 works

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References (105)

Draft Whole-Genome Sequence of the Biocontrol Agent Trichoderma harzianum T6776 Baroncelli, Riccardo; Piaggeschi, Giulia; Fiorini, Lisa Genome Announcements, Vol. 3, Issue 3 https://doi.org/10.1128/genomeA.00647-15	journal	June 2015
Deccan volcanism, the KT mass extinction and dinosaurs Keller, G.; Sahni, A.; Bajpai, S. Journal of Biosciences, Vol. 34, Issue 5 https://doi.org/10.1007/s12038-009-0059-6	journal	November 2009
Cerato-platanins: a fungal protein family with intriguing properties and application potential Gaderer, Romana; Bonazza, Klaus; Seidl-Seiboth, Verena Applied Microbiology and Biotechnology, Vol. 98, Issue 11 https://doi.org/10.1007/s00253-014-5690-y	journal	April 2014
Molecular diversity of LysM carbohydrate-binding motifs in fungi Akcapinar, Gunseli Bayram; Kappel, Lisa; Sezerman, Osman Ugur Current Genetics, Vol. 61, Issue 2 https://doi.org/10.1007/s00294-014-0471-9	journal	January 2015
Identification of the het-r vegetative incompatibility gene of Podospora anserina as a member of the fast evolving HNWD gene family Chevanne, Damien; Bastiaans, Eric; Debets, Alfons Current Genetics, Vol. 55, Issue 1 https://doi.org/10.1007/s00294-008-0227-5	journal	January 2009
Fungal Effector Proteins Stergiopoulos, Ioannis; de Wit, Pierre J. G. M. Annual Review of Phytopathology, Vol. 47, Issue 1 https://doi.org/10.1146/annurev.phyto.112408.132637	journal	September 2009
Wolbachia genomes: revealing the biology of parasitism and mutualism Fenn, Katelyn; Blaxter, Mark Trends in Parasitology, Vol. 22, Issue 2 https://doi.org/10.1016/j.pt.2005.12.012	journal	February 2006
Carbohydrate Binding Modules: Biochemical Properties and Novel Applications Shoseyov, O.; Shani, Z.; Levy, I. Microbiology and Molecular Biology Reviews, Vol. 70, Issue 2 https://doi.org/10.1128/MMBR.00028-05	journal	June 2006
Molecular evidence that the asexual industrial fungus Trichoderma reesei is a clonal derivative of the ascomycete Hypocrea jecorina. Kuhls, K.; Lieckfeldt, E.; Samuels, G. J. Proceedings of the National Academy of Sciences, Vol. 93, Issue 15, p. 7755-7760 https://doi.org/10.1073/pnas.93.15.7755	journal	July 1996
SignalP 4.0: discriminating signal peptides from transmembrane regions Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1701	journal	September 2011
Biodiversity of Trichoderma (Hypocreaceae) in Southern Europe and Macaronesia Jaklitsch, W. M.; Voglmayr, H. Studies in Mycology, Vol. 80 https://doi.org/10.1016/j.simyco.2014.11.001	journal	March 2015
Genome Sequence and Annotation of Trichoderma parareesei , the Ancestor of the Cellulase Producer Trichoderma reesei Yang, Dongqing; Pomraning, Kyle; Kopchinskiy, Alexey Genome Announcements, Vol. 3, Issue 4 https://doi.org/10.1128/genomeA.00885-15	journal	August 2015
Phylogenomic evolutionary surveys of subtilase superfamily genes in fungi Li, Juan; Gu, Fei; Wu, Runian Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep45456	journal	March 2017
The Genomes of Three Uneven Siblings: Footprints of the Lifestyles of Three Trichoderma Species Schmoll, Monika; Dattenböck, Christoph; Carreras-Villaseñor, Nohemí Microbiology and Molecular Biology Reviews, Vol. 80, Issue 1 https://doi.org/10.1128/MMBR.00040-15	journal	February 2016
Secondary metabolism in Trichoderma - a genomic perspective Mukherjee, P. K.; Horwitz, B. A.; Kenerley, C. M. Microbiology, Vol. 158, Issue 1 https://doi.org/10.1099/mic.0.053629-0	journal	October 2011
Hypocrea virens sp. nov., the teleomorph of Trichoderma virens Chaverri, Priscila; Samuels, Gary J.; Stewart, Elwin L. Mycologia, Vol. 93, Issue 6 https://doi.org/10.1080/00275514.2001.12063245	journal	November 2001
Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments Talavera, Gerard; Castresana, Jose Systematic Biology, Vol. 56, Issue 4 https://doi.org/10.1080/10635150701472164	journal	August 2007
The Trichoderma harzianum demon: complex speciation history resulting in coexistence of hypothetical biological species, recent agamospecies and numerous relict lineages Druzhinina, Irina S.; Kubicek, Christian P.; Komon-Zelazowska, Monika BMC Evolutionary Biology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2148-10-94	journal	January 2010
antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences Medema, Marnix H.; Blin, Kai; Cimermancic, Peter Nucleic Acids Research, Vol. 39, Issue suppl_2 https://doi.org/10.1093/nar/gkr466	journal	June 2011
Characterization of hch , the Podospora anserina homolog of the het-c heterokaryon incompatibility gene of Neurospora crassa Saupe, Sven J.; Clavé, Corinne; Sabourin, Martine Current Genetics, Vol. 38, Issue 1 https://doi.org/10.1007/s002940000130	journal	July 2000
CAFE: a computational tool for the study of gene family evolution De Bie, T.; Cristianini, N.; Demuth, J. P. Bioinformatics, Vol. 22, Issue 10 https://doi.org/10.1093/bioinformatics/btl097	journal	March 2006
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
An overview of the systematics of the Sordariomycetes based on a four-gene phylogeny Zhang, Ning; Castlebury, Lisa A.; Miller, Andrew N. Mycologia, Vol. 98, Issue 6 https://doi.org/10.1080/15572536.2006.11832635	journal	November 2006
Host-specific transcriptomic pattern of Trichoderma virens during interaction with maize or tomato roots Morán-Diez, Maria E.; Trushina, Naomi; Lamdan, Netta BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-014-1208-3	journal	January 2015
BEAST 2: A Software Platform for Bayesian Evolutionary Analysis Bouckaert, Remco; Heled, Joseph; Kühnert, Denise PLoS Computational Biology, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pcbi.1003537	journal	April 2014
Relationship between Phylogenetic Distribution and Genomic Features in Neurospora crassa Kasuga, Takao; Mannhaupt, Gertrud; Glass, N. Louise PLoS ONE, Vol. 4, Issue 4 https://doi.org/10.1371/journal.pone.0005286	journal	April 2009
Identification of Specificity Determinants and Generation of Alleles with Novel Specificity at the het-cHeterokaryon Incompatibility Locus of Neurospora crassa Wu, Jennifer; Glass, N. Louise Molecular and Cellular Biology, Vol. 21, Issue 4 https://doi.org/10.1128/MCB.21.4.1045-1057.2001	journal	February 2001
Cooler winters as a possible cause of mass extinctions at the Eocene/Oligocene boundary Ivany, Linda C.; Patterson, William P.; Lohmann, Kyger C. Nature, Vol. 407, Issue 6806 https://doi.org/10.1038/35038044	journal	October 2000
InterPro in 2017—beyond protein family and domain annotations Finn, Robert D.; Attwood, Teresa K.; Babbitt, Patricia C. Nucleic Acids Research, Vol. 45, Issue D1 https://doi.org/10.1093/nar/gkw1107	journal	November 2016
Comparative analysis of the Trichoderma reesei transcriptome during growth on the cellulase inducing substrates wheat straw and lactose Bischof, Robert; Fourtis, Lukas; Limbeck, Andreas Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-127	journal	January 2013
The Pfam protein families database: towards a more sustainable future Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1344	journal	December 2015
Draft Whole-Genome Sequence of Trichoderma gamsii T6085, a Promising Biocontrol Agent of Fusarium Head Blight on Wheat Baroncelli, Riccardo; Zapparata, Antonio; Piaggeschi, Giulia Genome Announcements, Vol. 4, Issue 1 https://doi.org/10.1128/genomeA.01747-15	journal	February 2016
The carbohydrate-active enzymes database (CAZy) in 2013 Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1178	journal	November 2013
Systematics of the Trichoderma harzianum species complex and the re-identification of commercial biocontrol strains Chaverri, Priscila; Branco-Rocha, Fabiano; Jaklitsch, Walter Mycologia, Vol. 107, Issue 3 https://doi.org/10.3852/14-147	journal	May 2015
Genome Annotation and Curation Using MAKER and MAKER‐P Campbell, Michael S.; Holt, Carson; Moore, Barry Current Protocols in Bioinformatics, Vol. 48, Issue 1 https://doi.org/10.1002/0471250953.bi0411s48	journal	December 2014
Intervene: a tool for intersection and visualization of multiple gene or genomic region sets Khan, Aziz; Mathelier, Anthony BMC Bioinformatics, Vol. 18, Issue 1 https://doi.org/10.1186/s12859-017-1708-7	journal	May 2017
Overlapping Podospora anserina Transcriptional Responses to Bacterial and Fungal Non Self Indicate a Multilayered Innate Immune Response Lamacchia, Marina; Dyrka, Witold; Breton, Annick Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00471	journal	April 2016
The evolutionary origin of orphan genes Tautz, Diethard; Domazet-Lošo, Tomislav Nature Reviews Genetics, Vol. 12, Issue 10 https://doi.org/10.1038/nrg3053	journal	August 2011
Fungal lifestyle reflected in serine protease repertoire Muszewska, Anna; Stepniewska-Dziubinska, Marta M.; Steczkiewicz, Kamil Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-09644-w	journal	August 2017
Ankyrin Repeat: A Unique Motif Mediating Protein−Protein Interactions ^† Li, Junan; Mahajan, Anjali; Tsai, Ming-Daw Biochemistry, Vol. 45, Issue 51 https://doi.org/10.1021/bi062188q	journal	December 2006
European species of Hypocrea Part I. The green-spored species Jaklitsch, Walter M. Studies in Mycology, Vol. 63 https://doi.org/10.3114/sim.2009.63.01	journal	January 2009
Variance to Mean Ratio, R(t), for Poisson Processes on Phylogenetic Trees Goldman, Nick Molecular Phylogenetics and Evolution, Vol. 3, Issue 3 https://doi.org/10.1006/mpev.1994.1025	journal	September 1994
Sexual selection in fungi Nieuwenhuis, B. P. S.; Aanen, D. K. Journal of Evolutionary Biology, Vol. 25, Issue 12 https://doi.org/10.1111/jeb.12017	journal	November 2012
Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes: EVOLUTIONARY ORIGIN OF GRASS-ASSOCIATED FUNGI Spatafora, J. W.; Sung, G. -H.; Sung, J. -M. Molecular Ecology, Vol. 16, Issue 8 https://doi.org/10.1111/j.1365-294X.2007.03225.x	journal	March 2007
Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma Kubicek, Christian P.; Herrera-Estrella, Alfredo; Seidl-Seiboth, Verena Genome Biology, Vol. 12, Issue 4 https://doi.org/10.1186/gb-2011-12-4-r40	journal	April 2011
Hypocrea atroviridis sp. nov., the teleomorph of Trichoderma atroviride Dodd, Sarah L.; Lieckfeldt, Elke; Samuels, Gary J. Mycologia, Vol. 95, Issue 1 https://doi.org/10.1080/15572536.2004.11833129	journal	January 2003
Mechanisms and Dynamics of Orphan Gene Emergence in Insect Genomes Wissler, Lothar; Gadau, Jürgen; Simola, Daniel F. Genome Biology and Evolution, Vol. 5, Issue 2 https://doi.org/10.1093/gbe/evt009	journal	January 2013
MycoCosm portal: gearing up for 1000 fungal genomes Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1183	journal	December 2013
Trichoderma: the genomics of opportunistic success Druzhinina, Irina S.; Seidl-Seiboth, Verena; Herrera-Estrella, Alfredo Nature Reviews Microbiology, Vol. 9, Issue 10 https://doi.org/10.1038/nrmicro2637	journal	September 2011
Investigating the beneficial traits of Trichoderma hamatum GD12 for sustainable agriculture—insights from genomics Studholme, David J.; Harris, Beverley; Le Cocq, Kate Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00258	journal	January 2013
Fungal incompatibility: Evolutionary origin in pathogen defense? Paoletti, Mathieu; Saupe, Sven J. BioEssays, Vol. 31, Issue 11 https://doi.org/10.1002/bies.200900085	journal	November 2009
Origin and evolution of carnivorism in the Ascomycota (fungi) Yang, E.; Xu, L.; Yang, Y. Proceedings of the National Academy of Sciences, Vol. 109, Issue 27 https://doi.org/10.1073/pnas.1120915109	journal	June 2012
Independent Expansion of Zincin Metalloproteinases in Onygenales Fungi May Be Associated with Their Pathogenicity Li, Juan; Zhang, Ke-Qin PLoS ONE, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pone.0090225	journal	February 2014
Sm1, a Proteinaceous Elicitor Secreted by the Biocontrol Fungus Trichoderma virens Induces Plant Defense Responses and Systemic Resistance Djonović, Slavica; Pozo, Maria J.; Dangott, Lawrence J. Molecular Plant-Microbe Interactions®, Vol. 19, Issue 8 https://doi.org/10.1094/MPMI-19-0838	journal	August 2006
Accelerated evolution associated with genome reduction in a free-living prokaryote Dufresne, Alexis; Garczarek, Laurence; Partensky, Frédéric Genome Biology, Vol. 6, Issue 2, p. R14 https://doi.org/10.1186/gb-2005-6-2-r14	journal	January 2005
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs Simão, Felipe A.; Waterhouse, Robert M.; Ioannidis, Panagiotis Bioinformatics, Vol. 31, Issue 19 https://doi.org/10.1093/bioinformatics/btv351	journal	June 2015
The ankyrin repeat as molecular architecture for protein recognition Mosavi, Leila K.; Cammett, Tobin J.; Desrosiers, Daniel C. Protein Science, Vol. 13, Issue 6 https://doi.org/10.1110/ps.03554604	journal	June 2004
Fungal Proliferation at the Cretaceous-Tertiary Boundary Vajda, V. Science, Vol. 303, Issue 5663 https://doi.org/10.1126/science.1093807	journal	March 2004
Causes and Consequences of Genome Expansion in Fungi Kelkar, Yogeshwar D.; Ochman, Howard Genome Biology and Evolution, Vol. 4, Issue 1 https://doi.org/10.1093/gbe/evr124	journal	November 2011
Fungal arabinan and l-arabinose metabolism Seiboth, Bernhard; Metz, Benjamin Applied Microbiology and Biotechnology, Vol. 89, Issue 6 https://doi.org/10.1007/s00253-010-3071-8	journal	January 2011
A complete annotation of the chromosomes of the cellulase producer Trichoderma reesei provides insights in gene clusters, their expression and reveals genes required for fitness Druzhinina, Irina S.; Kopchinskiy, Alexey G.; Kubicek, Eva M. Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0488-z	journal	March 2016
A comprehensive evolutionary classification of proteins encoded in complete eukaryotic genomes Koonin, Eugene V.; Fedorova, Natalie D.; Jackson, John D. Genome Biology, Vol. 5, Issue 2 https://doi.org/10.1186/gb-2004-5-2-r7	journal	January 2004
OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes Li, L. Genome Research, Vol. 13, Issue 9 https://doi.org/10.1101/gr.1224503	journal	September 2003
Trichoderma reesei complete genome sequence, repeat-induced point mutation, and partitioning of CAZyme gene clusters Li, Wan-Chen; Huang, Chien-Hao; Chen, Chia-Ling Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0825-x	journal	July 2017
Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts Druzhinina, Irina S.; Chenthamara, Komal; Zhang, Jian PLOS Genetics, Vol. 14, Issue 4 https://doi.org/10.1371/journal.pgen.1007322	journal	April 2018
Strong Genome-Wide Selection Early in the Evolution of Prochlorococcus Resulted in a Reduced Genome through the Loss of a Large Number of Small Effect Genes Sun, Zhiyi; Blanchard, Jeffrey L. PLoS ONE, Vol. 9, Issue 3 https://doi.org/10.1371/journal.pone.0088837	journal	March 2014
CDD: NCBI's conserved domain database Marchler-Bauer, Aron; Derbyshire, Myra K.; Gonzales, Noreen R. Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1221	journal	November 2014
Regulation and Role of Fungal Secondary Metabolites Macheleidt, Juliane; Mattern, Derek J.; Fischer, Juliane Annual Review of Genetics, Vol. 50, Issue 1 https://doi.org/10.1146/annurev-genet-120215-035203	journal	November 2016
Identification of mycoparasitism-related genes against the phytopathogen Sclerotinia sclerotiorum through transcriptome and expression profile analysis in Trichoderma harzianum Steindorff, Andrei Stecca; Ramada, Marcelo Henrique Soller; Coelho, Alexandre Siqueira Guedes BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-204	journal	March 2014
Sm2, a paralog of the Trichoderma cerato-platanin elicitor Sm1, is also highly important for plant protection conferred by the fungal-root interaction of Trichoderma with maize Gaderer, Romana; Lamdan, Netta L.; Frischmann, Alexa BMC Microbiology, Vol. 15, Issue 1 https://doi.org/10.1186/s12866-014-0333-0	journal	January 2015
Whole genome comparison of the A. fumigatus family Wortman, J. R.; Fedorova, N.; Crabtree, J. Medical Mycology, Vol. 44, Issue s1 https://doi.org/10.1080/13693780600835799	journal	January 2006
Molecular Genetics of Heterokaryon Incompatibility in Filamentous Ascomycetes Saupe, S. J. Microbiology and Molecular Biology Reviews, Vol. 64, Issue 3 https://doi.org/10.1128/MMBR.64.3.489-502.2000	journal	September 2000
The structure of the negative transcriptional regulator NmrA reveals a structural superfamily which includes the short-chain dehydrogenase/reductases Stammers, D. K. The EMBO Journal, Vol. 20, Issue 23 https://doi.org/10.1093/emboj/20.23.6619	journal	December 2001
CAZyme content of Pochonia chlamydosporia reflects that chitin and chitosan modification are involved in nematode parasitism: CAZome of Pochonia chlamydosporia Aranda-Martinez, Almudena; Lenfant, Nicolas; Escudero, Nuria Environmental Microbiology, Vol. 18, Issue 11 https://doi.org/10.1111/1462-2920.13544	journal	October 2016
Molecular reidentification of human pathogenic Trichoderma isolates as Trichoderma longibrachiatum and Trichoderma citrinoviride Kuhls, K.; Lieckfeldt, E.; BÖrner, T. Medical Mycology, Vol. 37, Issue 1 https://doi.org/10.1080/02681219980000041	journal	January 1999
Genome sequence of Trichoderma virens FT-333 from tropical marine climate Kuo, Hsiao-Che; Wang, Ting-Yu; Chen, Peng-Peng FEMS Microbiology Letters, Vol. 362, Issue 7 https://doi.org/10.1093/femsle/fnv036	journal	March 2015
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro Molecular Biology and Evolution, Vol. 33, Issue 7 https://doi.org/10.1093/molbev/msw054	journal	March 2016
Draft Genome Sequence of a Strain of Cosmopolitan Fungus Trichoderma atroviride Shi-Kunne, Xiaoqian; Seidl, Michael F.; Faino, Luigi Genome Announcements, Vol. 3, Issue 3 https://doi.org/10.1128/genomeA.00287-15	journal	May 2015
The oldest fossil evidence of animal parasitism by fungi supports a Cretaceous diversification of fungal–arthropod symbioses Sung, Gi-Ho; Poinar, George O.; Spatafora, Joseph W. Molecular Phylogenetics and Evolution, Vol. 49, Issue 2 https://doi.org/10.1016/j.ympev.2008.08.028	journal	November 2008
Evolution and Ecophysiology of the Industrial Producer Hypocrea jecorina (Anamorph Trichoderma reesei) and a New Sympatric Agamospecies Related to It Druzhinina, Irina S.; Komoń-Zelazowska, Monika; Atanasova, Lea PLoS ONE, Vol. 5, Issue 2 https://doi.org/10.1371/journal.pone.0009191	journal	February 2010
Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus de Vries, Ronald P.; Riley, Robert; Wiebenga, Ad Genome Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s13059-017-1151-0	journal	February 2017
Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina) Martinez, Diego; Berka, Randy M.; Henrissat, Bernard Nature Biotechnology, Vol. 26, Issue 5 https://doi.org/10.1038/nbt1403	journal	May 2008
Proto-genes and de novo gene birth Carvunis, Anne-Ruxandra; Rolland, Thomas; Wapinski, Ilan Nature, Vol. 487, Issue 7407 https://doi.org/10.1038/nature11184	journal	June 2012
Proteinortho: Detection of (Co-)orthologs in large-scale analysis Lechner, Marcus; Findeiß, Sven; Steiner, Lydia BMC Bioinformatics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2105-12-124	journal	April 2011
Three species of Hypomyces growing on basidiomata of Stereaceae Põldmaa, Kadri Mycologia, Vol. 95, Issue 5 https://doi.org/10.1080/15572536.2004.11833051	journal	September 2003
Comparative Genomics Provide Insights into Evolution of Trichoderma Nutrition Style Xie, Bin-Bin; Qin, Qi-Long; Shi, Mei Genome Biology and Evolution, Vol. 6, Issue 2 https://doi.org/10.1093/gbe/evu018	journal	January 2014
Polysaccharide lyases Sutherland, Ian W. FEMS Microbiology Reviews, Vol. 16, Issue 4 https://doi.org/10.1111/j.1574-6976.1995.tb00179.x	journal	July 1995
Hypocrea virens sp. nov., the Teleomorph of Trichoderma virens Chaverri, Priscila; Samuels, Gary J.; Stewart, Elwin L. Mycologia, Vol. 93, Issue 6 https://doi.org/10.2307/3761672	journal	November 2001
An overview of the systematics of the Sordariomycetes based on a four-gene phylogeny Zhang, N.; Castlebury, L. A.; Miller, A. N. Mycologia, Vol. 98, Issue 6 https://doi.org/10.3852/mycologia.98.6.1076	journal	November 2006
Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins Carim, Sean; Azadeh, Ashley L.; Kazakov, Alexey E. The ISME Journal, Vol. 15, Issue 8 https://doi.org/10.1038/s41396-021-00921-1	journal	March 2021
An SHR–SCR module specifies legume cortical cell fate to enable nodulation Dong, Wentao; Zhu, Yayun; Chang, Huizhong Nature, Vol. 589, Issue 7843 https://doi.org/10.1038/s41586-020-3016-z	journal	December 2020
A gene expression atlas for different kinds of stress in the mouse brain Flati, Tiziano; Gioiosa, Silvia; Chillemi, Giovanni Scientific Data, Vol. 7, Issue 1 https://doi.org/10.1038/s41597-020-00772-z	journal	December 2020
Genome-scale model reconstruction of the methylotrophic yeast Ogataea polymorpha Liebal, Ulf Winfried; Fabry, Brigida A.; Ravikrishnan, Aarthi RWTH Aachen University https://doi.org/10.18154/rwth-2021-02761	text	January 2021
Three Species of Hypomyces Growing on Basidiomata of Stereaceae Poldmaa, Kadri Mycologia, Vol. 95, Issue 5 https://doi.org/10.2307/3762020	journal	September 2003
BEAST 2: A Software Platform for Bayesian Evolutionary Analysis Remco, Bouckaert,; Joseph, Heled,; Denise, Kühnert, ETH Zurich https://doi.org/10.3929/ethz-b-000085272	text	January 2014
Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus Vries, R. P. De; Riley, R.; Wiebenga, A. Karlsruhe https://doi.org/10.5445/ir/1000067295	text	January 2017
Hypocrea atroviridis sp. nov., the Teleomorph of Trichoderma atroviride Dodd, Sarah L.; Lieckfeldt, Elke; Samuels, Gary J. Mycologia, Vol. 95, Issue 1 https://doi.org/10.2307/3761959	journal	January 2003
Plasmodium telomeres: a pathogen's perspective Scherf, A. Current Opinion in Microbiology, Vol. 4, Issue 4 https://doi.org/10.1016/s1369-5274(00)00227-7	journal	August 2001
Characterization and phylogenetic analysis of the complete mitochondrial genome of the pathogenic fungus Ilyonectria destructans Androsiuk, Piotr; Okorski, Adam; Paukszto, Łukasz Scientific Reports, Vol. 12, Issue 1 https://doi.org/10.1038/s41598-022-05428-z	journal	February 2022
Full-length transcriptome analysis of multiple organs and identification of adaptive genes and pathways in Mikania micrantha Ruan, Xiaoxian; Wang, Zhen; Su, Yingjuan Scientific Reports, Vol. 12, Issue 1 https://doi.org/10.1038/s41598-022-07198-0	journal	February 2022
l- xylo -3-Hexulose Reductase Is the Missing Link in the Oxidoreductive Pathway for d-Galactose Catabolism in Filamentous Fungi Mojzita, Dominik; Herold, Silvia; Metz, Benjamin Journal of Biological Chemistry, Vol. 287, Issue 31 https://doi.org/10.1074/jbc.m112.372755	journal	May 2012
Bayesian Phylogenetic Estimation of Clade Ages Supports Trans-Atlantic Dispersal of Cichlid Fishes Matschiner, Michael; Musilová, Zuzana; Barth, Julia M. I. Systematic Biology https://doi.org/10.1093/sysbio/syw076	journal	August 2016
EVOLUTION OF HABITAT PREFERENCE AND NUTRITION MODE IN A COSMOPOLITAN FUNGAL GENUS WITH EVIDENCE OF INTERKINGDOM HOST JUMPS AND MAJOR SHIFTS IN ECOLOGY: TRICHODERMA EVOLUTION Chaverri, Priscila; Samuels, Gary J. Evolution https://doi.org/10.1111/evo.12169	journal	June 2013
Correction for Compant et al., “Draft Genome Sequence of the Root-Colonizing Fungus Trichoderma harzianum B97” Compant, Stéphane; Gerbore, Jonathan; Antonielli, Livio Genome Announcements, Vol. 5, Issue 23 https://doi.org/10.1128/genomea.00549-17	journal	June 2017
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Additional file 10: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267060 The current record is supplemented by this text	text	January 2019
Additional file 11: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267069 The current record is supplemented by this dataset	dataset	January 2019
Additional file 11: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267069.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional file 12: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267078 The current record is supplemented by this text	text	January 2019
Additional file 12: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267078.v1 The current record is supplemented by this text	text	January 2019
Additional file 13: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267081 The current record is supplemented by this text	text	January 2019
Additional file 13: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267081.v1 The current record is supplemented by this text	text	January 2019
Additional file 14: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267084 The current record is supplemented by this text	text	January 2019
Additional file 14: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267084.v1 The current record is supplemented by this text	text	January 2019
Additional file 15: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267087 The current record is supplemented by this dataset	dataset	January 2019
Additional file 15: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267087.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional file 16: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267090.v1 The current record is supplemented by this text	text	January 2019
Additional file 17: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267093.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional file 18: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267096 The current record is supplemented by this text	text	January 2019
Additional file 18: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267096.v1 The current record is supplemented by this text	text	January 2019
Additional file 1: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267102 The current record is supplemented by this dataset	dataset	January 2019
Additional file 20: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267105 The current record is supplemented by this dataset	dataset	January 2019
Additional file 20: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267105.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional file 21: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267108 The current record is supplemented by this dataset	dataset	January 2019
Additional file 21: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267108.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional file 3: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267120 The current record is supplemented by this dataset	dataset	January 2019
Additional file 3: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267120.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional file 4: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267129.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional file 5: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267135 The current record is supplemented by this dataset	dataset	January 2019
Additional file 6: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267144 The current record is supplemented by this dataset	dataset	January 2019
Additional file 6: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267144.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional File 7: Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267153 The current record is supplemented by this dataset	dataset	January 2019
Additional file 8: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267159 The current record is supplemented by this dataset	dataset	January 2019
Additional file 8: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267159.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional file 9: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267162 The current record is supplemented by this text	text	January 2019
Additional file 9: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267162.v1 The current record is supplemented by this text	text	January 2019
Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.c.4539917 The current record is supplemented by this collection	collection	January 2019
Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.c.4539917.v1 The current record is supplemented by this collection	collection	January 2019
Additional File 7: Reaney, Ashley; Saldarriaga-Cรณrdoba, Mรณnica; Pincheira-Donoso, Daniel https://doi.org/10.6084/m9.figshare.5863017 The current record is supplemented by this image	image	January 2018
Additional file 16: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267090 The current record is supplemented by this text	text	January 2019
Additional file 17: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267093 The current record is supplemented by this dataset	dataset	January 2019
Additional file 19: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267099.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional file 1: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267102.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional file 2: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267111 The current record is supplemented by this text	text	January 2019
Additional file 4: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267129 The current record is supplemented by this dataset	dataset	January 2019
Additional file 5: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267135.v1 The current record is supplemented by this dataset	dataset	January 2019
Additional File 7: Uyhelji, Hilary; Kupfer, Doris; White, Vicky https://doi.org/10.6084/m9.figshare.6234338 The current record is supplemented by this dataset	dataset	January 2018
Additional file 10: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267060.v1 The current record is supplemented by this text	text	January 2019
Additional file 2: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267111.v1 The current record is supplemented by this text	text	January 2019
Additional File 7: Lu, Zhen; Huang, Qingyang; Zhang, Tong https://doi.org/10.6084/m9.figshare.6600605.v1 The current record is supplemented by this dataset	dataset	January 2018
Additional file 19: of Evolution and comparative genomics of the most common Trichoderma species Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267099 The current record is supplemented by this dataset	dataset	January 2019
Additional File 7: Reaney, Ashley; Saldarriaga-Cรณrdoba, Mรณnica; Pincheira-Donoso, Daniel https://doi.org/10.6084/m9.figshare.5863017.v1 The current record is supplemented by this image	image	January 2018
Additional File 7: Kubicek, Christian; Steindorff, Andrei; Chenthamara, Komal https://doi.org/10.6084/m9.figshare.8267153.v1 The current record is supplemented by this dataset	dataset	January 2019