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; Atanasova, Lea; Yang, Dongqing; Miao, Youzhi; Rahimi, Mohammad J.; Grujic, Marica; Cai, Feng; Pourmehdi, Shadi; Salim, Kamariah Abu; Pretzer, Carina; Kopchinskiy, Alexey G.; Henrissat, Bernard; Kuo, Alan; Hundley, Hope; Wang, Mei; Aerts, Andrea; Salamov, Asaf; Lipzen, Anna; LaButti, Kurt; Barry, Kerrie; Grigoriev, Igor V.; Shen, Qirong; Kubicek, Christian P.; Martin, Francis

doi:10.1371/journal.pgen.1007322

Title: Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts

Journal Article · Mon Apr 09 00:00:00 EDT 2018 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1007322· OSTI ID:1544030

^[1]; Chenthamara, Komal ^[1]; Zhang, Jian ^[2]; Atanasova, Lea ^[3]; Yang, Dongqing ^[4]; Miao, Youzhi ^[4];

^[1]; Grujic, Marica ^[1];

^[5]; Pourmehdi, Shadi ^[1];

^[6]; Pretzer, Carina ^[1]; Kopchinskiy, Alexey G. ^[1];

^[7];

^[8]; Hundley, Hope ^[8]; Wang, Mei ^[8]; Aerts, Andrea ^[8]; Salamov, Asaf ^[8]; Lipzen, Anna ^[8] more »

TU Wien, Vienna (Austria)
Nanjing Univ. (China)
TU Wien, Vienna (Austria); Univ. of Natural Resources and Life Sciences–BOKU, Vienna (Austria)
Nanjing Agricultural Univ., Nanjing (China)
TU Wien, Vienna (Austria); Nanjing Agricultural Univ., Nanjing (China)
Univ. Brunei Brunei (Darussalam)
Aix-Marseille Univ., Marseille (France); INRA, USC, Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
(France)

Unlike most other fungi, molds of the genus Trichoderma (Hypocreales, Ascomycota) are aggressive parasites of other fungi and efficient decomposers of plant biomass. Although nutritional shifts are common among hypocrealean fungi, there are no examples of such broad substrate versatility as that observed in Trichoderma. A phylogenomic analysis of 23 hypocrealean fungi (including nine Trichoderma spp. and the related Escovopsis weberi) revealed that the genus Trichoderma has evolved from an ancestor with limited cellulolytic capability that fed on either fungi or arthropods. The evolutionary analysis of Trichoderma genes encoding plant cell wall-degrading carbohydrate-active enzymes and auxiliary proteins (pcwdCAZome, 122 gene families) based on a gene tree / species tree reconciliation demonstrated that the formation of the genus was accompanied by an unprecedented extent of lateral gene transfer (LGT). Nearly one-half of the genes in Trichoderma pcwdCAZome (41%) were obtained via LGT from plant-associated filamentous fungi belonging to different classes of Ascomycota, while no LGT was observed from other potential donors. In addition to the ability to feed on unrelated fungi (such as Basidiomycota), we also showed that Trichoderma is capable of endoparasitism on a broad range of Ascomycota, including extant LGT donors. This phenomenon was not observed in E. weberi and rarely in other mycoparasitic hypocrealean fungi. Thus, our study suggests that LGT is linked to the ability of Trichoderma to parasitize taxonomically related fungi (up to adelphoparasitism in strict sense). This may have allowed primarily mycotrophic Trichoderma fungi to evolve into decomposers of plant biomass.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); Austrian Science Fund (FWF); National Natural Science Foundation of China (NSFC); Chinese Ministry of Science and Technology

Grant/Contract Number:: AC02-05CH11231; P25613-B20; WWTF-LS13-048; 31330069; 2015CB150500

OSTI ID:: 1544030

Alternate ID(s):: OSTI ID: 1619097

Journal Information:: PLoS Genetics, Vol. 14, Issue 4; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 71 works

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References (105)

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
Plant Cell Wall–Degrading Enzymes and Their Secretion in Plant-Pathogenic Fungi Kubicek, Christian P.; Starr, Trevor L.; Glass, N. Louise Annual Review of Phytopathology, Vol. 52, Issue 1 https://doi.org/10.1146/annurev-phyto-102313-045831	journal	August 2014
Genetically Closely Related but Phenotypically Divergent Trichoderma Species Cause Green Mold Disease in Oyster Mushroom Farms Worldwide Komon-Zelazowska, M.; Bissett, J.; Zafari, D. Applied and Environmental Microbiology, Vol. 73, Issue 22 https://doi.org/10.1128/aem.01059-07	journal	September 2007
Fungal Cellulases Payne, Christina M.; Knott, Brandon C.; Mayes, Heather B. Chemical Reviews, Vol. 115, Issue 3 https://doi.org/10.1021/cr500351c	journal	January 2015
Experimental mixture design as a tool to enhance glycosyl hydrolases production by a new Trichoderma harzianum P49P11 strain cultivated under controlled bioreactor submerged fermentation da Silva Delabona, Priscila; Sanchez Farinas, Cristiane; da Silva Lima, Deise Juliana Bioresource Technology, Vol. 132 https://doi.org/10.1016/j.biortech.2012.11.087	journal	March 2013
Genome sequence of the insect pathogenic fungus Cordyceps militaris, a valued traditional chinese medicine Zheng, Peng; Xia, Yongliang; Xiao, Guohua Genome Biology, Vol. 12, Issue 11 https://doi.org/10.1186/gb-2011-12-11-r116	journal	January 2011
Cellulases and beyond: the first 70 years of the enzyme producer Trichoderma reesei Bischof, Robert H.; Ramoni, Jonas; Seiboth, Bernhard Microbial Cell Factories, Vol. 15, Issue 1 https://doi.org/10.1186/s12934-016-0507-6	journal	June 2016
Reconciliation with non-binary species trees. Vernot, Benjamin; Stolzer, Maureen; Goldman, Aiton Carnegie Mellon University https://doi.org/10.1184/r1/6104126	text	January 2008
Gene transfer from a parasitic flowering plant to a fern Davis, Charles C.; Anderson, William R.; Wurdack, Kenneth J. Proceedings of the Royal Society B: Biological Sciences, Vol. 272, Issue 1578 https://doi.org/10.1098/rspb.2005.3226	journal	September 2005
Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis Castresana, J. Molecular Biology and Evolution, Vol. 17, Issue 4 https://doi.org/10.1093/oxfordjournals.molbev.a026334	journal	April 2000
Regulation of Morphogenesis and Biocontrol Properties in Trichoderma virens by a VELVET Protein, Vel1 Mukherjee, P. K.; Kenerley, C. M. Applied and Environmental Microbiology, Vol. 76, Issue 7 https://doi.org/10.1128/aem.02391-09	journal	February 2010
The neutral theory of molecular evolution and the world view of the neutralists Kimura, Motoo Genome, Vol. 31, Issue 1 https://doi.org/10.1139/g89-009	journal	January 1989
High-quality draft assemblies of mammalian genomes from massively parallel sequence data Gnerre, S.; MacCallum, I.; Przybylski, D. Proceedings of the National Academy of Sciences, Vol. 108, Issue 4 https://doi.org/10.1073/pnas.1017351108	journal	December 2010
Furcation and fusion: The phylogenetics of evolutionary novelty Oakley, Todd H. Developmental Biology, Vol. 431, Issue 1 https://doi.org/10.1016/j.ydbio.2017.09.015	journal	November 2017
Expanding horizons through chromosome exchange van Ooij, Christiaan Nature Reviews Microbiology, Vol. 8, Issue 5 https://doi.org/10.1038/nrmicro2357	journal	May 2010
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
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
The Role of Horizontal Gene Transfer in the Evolution of the Oomycetes Savory, Fiona; Leonard, Guy; Richards, Thomas A. PLOS Pathogens, Vol. 11, Issue 5 https://doi.org/10.1371/journal.ppat.1004805	journal	May 2015
The genome sequence of the filamentous fungus Neurospora crassa Galagan, James E.; Calvo, Sarah E.; Borkovich, Katherine A. Nature, Vol. 422, Issue 6934 https://doi.org/10.1038/nature01554	journal	April 2003
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
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
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Inferring duplications, losses, transfers and incomplete lineage sorting with nonbinary species trees. Stolzer, Maureen; Lai, Han; Xu, Minli Carnegie Mellon University https://doi.org/10.1184/r1/6099671	text	January 2012
Rnnotator: an automated de novo transcriptome assembly pipeline from stranded RNA-Seq reads Martin, Jeffrey; Bruno, Vincent M.; Fang, Zhide BMC Genomics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2164-11-663	journal	January 2010
Comparative Pathogenomics Reveals Horizontally Acquired Novel Virulence Genes in Fungi Infecting Cereal Hosts Gardiner, Donald M.; McDonald, Megan C.; Covarelli, Lorenzo ETH Zurich https://doi.org/10.3929/ethz-b-000057696	text	January 2012
Red Algae Lose Key Mitochondrial Genes in Response to Becoming Parasitic Hancock, Lillian; Goff, Lynda; Lane, Christopher Genome Biology and Evolution, Vol. 2 https://doi.org/10.1093/gbe/evq075	journal	January 2010
The simple-septate basidiomycetes: a synopsis Bauer, Robert; Begerow, Dominik; Sampaio, José Paulo Mycological Progress, Vol. 5, Issue 1 https://doi.org/10.1007/s11557-006-0502-0	journal	March 2006
TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops Milne, I.; Lindner, D.; Bayer, M. Bioinformatics, Vol. 25, Issue 1 https://doi.org/10.1093/bioinformatics/btn575	journal	November 2008
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
The Genome of Nectria haematococca: Contribution of Supernumerary Chromosomes to Gene Expansion Coleman, Jeffrey J.; Rounsley, Steve D.; Rodriguez-Carres, Marianela PLoS Genetics, Vol. 5, Issue 8 https://doi.org/10.1371/journal.pgen.1000618	journal	August 2009
The Evolution of Fungal Metabolic Pathways Wisecaver, Jennifer H.; Slot, Jason C.; Rokas, Antonis PLoS Genetics, Vol. 10, Issue 12 https://doi.org/10.1371/journal.pgen.1004816	journal	December 2014
Clustal W and Clustal X version 2.0 Larkin, M. A.; Blackshields, G.; Brown, N. P. Bioinformatics, Vol. 23, Issue 21, p. 2947-2948 https://doi.org/10.1093/bioinformatics/btm404	journal	September 2007
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
Green Mold Diseases of Agaricus and Pleurotus spp. Are Caused by Related but Phylogenetically Different Trichoderma Species Hatvani, L.; Antal, Z.; Manczinger, L. Phytopathology, Vol. 97, Issue 4 https://doi.org/10.1094/phyto-97-4-0532	journal	April 2007
Fungal metabolic gene clustersâ€”caravans traveling across genomes and environments Wisecaver, Jennifer H.; Rokas, Antonis Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00161	journal	March 2015
Plant-Symbiotic Fungi as Chemical Engineers: Multi-Genome Analysis of the Clavicipitaceae Reveals Dynamics of Alkaloid Loci Schardl, Christopher L.; Young, Carolyn A.; Hesse, Uljana PLoS Genetics, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pgen.1003323	journal	February 2013
Genome Sequencing and Comparative Transcriptomics of the Model Entomopathogenic Fungi Metarhizium anisopliae and M. acridum Gao, Qiang; Jin, Kai; Ying, Sheng-Hua PLoS Genetics, Vol. 7, Issue 1 https://doi.org/10.1371/journal.pgen.1001264	journal	January 2011
Trichoderma pseudokoningii as a Cause of Fatal Infection in a Bone Marrow Transplant Recipient Gautheret, A.; Dromer, F.; Bourhis, J. -H. Clinical Infectious Diseases, Vol. 20, Issue 4 https://doi.org/10.1093/clinids/20.4.1063	journal	April 1995
Comparative Pathogenomics Reveals Horizontally Acquired Novel Virulence Genes in Fungi Infecting Cereal Hosts Gardiner, Donald M.; McDonald, Megan C.; Covarelli, Lorenzo PLoS Pathogens, Vol. 8, Issue 9 https://doi.org/10.1371/journal.ppat.1002952	journal	September 2012
Acquisition of prokaryotic genes by fungal genomes Marcet-Houben, Marina; Gabaldón, Toni Trends in Genetics, Vol. 26, Issue 1 https://doi.org/10.1016/j.tig.2009.11.007	journal	January 2010
ProtTest 3: fast selection of best-fit models of protein evolution Darriba, Diego; Taboada, Guillermo L.; Doallo, Ramón Bioinformatics, Vol. 27, Issue 8 https://doi.org/10.1093/bioinformatics/btr088	journal	February 2011
MRBAYES: Bayesian inference of phylogenetic trees Huelsenbeck, J. P.; Ronquist, F. Bioinformatics, Vol. 17, Issue 8 https://doi.org/10.1093/bioinformatics/17.8.754	journal	August 2001
Transformants of Trichoderma longibrachiatum Overexpressing the β-1,4-Endoglucanase Gene egl1 Show Enhanced Biocontrol of Pythium ultimum on Cucumber Migheli, Quirico; González-Candelas, Luis; Dealessi, Laura Phytopathology, Vol. 88, Issue 7 https://doi.org/10.1094/PHYTO.1998.88.7.673	journal	July 1998
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
Small genome of the fungus Escovopsis weberi , a specialized disease agent of ant agriculture de Man, Tom J. B.; Stajich, Jason E.; Kubicek, Christian P. Proceedings of the National Academy of Sciences, Vol. 113, Issue 13 https://doi.org/10.1073/pnas.1518501113	journal	March 2016
Diversity of fungal endophytes in leaves and stems of wild rubber trees (Hevea brasiliensis) in Peru Gazis, Romina; Chaverri, Priscila Fungal Ecology, Vol. 3, Issue 3 https://doi.org/10.1016/j.funeco.2009.12.001	journal	August 2010
Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes Levasseur, Anthony; Drula, Elodie; Lombard, Vincent Biotechnology for Biofuels, Vol. 6, Issue 1, Article No. 41 https://doi.org/10.1186/1754-6834-6-41	journal	January 2013
Horizontal Transfer of a Nitrate Assimilation Gene Cluster and Ecological Transitions in Fungi: A Phylogenetic Study Slot, Jason C.; Hibbett, David S. PLoS ONE, Vol. 2, Issue 10 https://doi.org/10.1371/journal.pone.0001097	journal	October 2007
Funybase: a Fungal phylogenomic database Marthey, Sylvain; Aguileta, Gabriela; Rodolphe, Francois BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-456	journal	January 2008
Reconciliation with Non-Binary Species Trees Vernot, Benjamin; Stolzer, Maureen; Goldman, Aiton Journal of Computational Biology, Vol. 15, Issue 8 https://doi.org/10.1089/cmb.2008.0092	journal	October 2008
NOTUNG: a program for dating gene duplications and optimizing gene family trees. Chen, Kevin; Durand, Dannie; Farach-Colton, Martin Figshare https://doi.org/10.1184/r1/6103910.v1	text	January 2018
Genera in Bionectriaceae, Hypocreaceae, and Nectriaceae (Hypocreales) proposed for acceptance or rejection Rossman, Amy Y.; Seifert, Keith A.; Samuels, Gary J. IMA Fungus, Vol. 4, Issue 1 https://doi.org/10.5598/imafungus.2013.04.01.05	journal	April 2013
Inferring duplications, losses, transfers and incomplete lineage sorting with nonbinary species trees Stolzer, Maureen; Lai, Han; Xu, Minli Bioinformatics, Vol. 28, Issue 18 https://doi.org/10.1093/bioinformatics/bts386	journal	September 2012
Deciphering the Cryptic Genome: Genome-wide Analyses of the Rice Pathogen Fusarium fujikuroi Reveal Complex Regulation of Secondary Metabolism and Novel Metabolites Wiemann, Philipp; Sieber, Christian M. K.; von Bargen, Katharina W. PLoS Pathogens, Vol. 9, Issue 6 https://doi.org/10.1371/journal.ppat.1003475	journal	June 2013
MrBayes 3: Bayesian phylogenetic inference under mixed models Ronquist, Fredrik; Huelsenbeck, John P. Bioinformatics, Vol. 19, Issue 12, p. 1572-1574 https://doi.org/10.1093/bioinformatics/btg180	journal	August 2003
Swollenin from Trichoderma reesei exhibits hydrolytic activity against cellulosic substrates with features of both endoglucanases and cellobiohydrolases Andberg, Martina; Penttilä, Merja; Saloheimo, Markku Bioresource Technology, Vol. 181 https://doi.org/10.1016/j.biortech.2015.01.024	journal	April 2015
Signal Transduction by Tga3, a Novel G Protein Subunit of Trichoderma atroviride Zeilinger, S.; Reithner, B.; Scala, V. Applied and Environmental Microbiology, Vol. 71, Issue 3 https://doi.org/10.1128/aem.71.3.1591-1597.2005	journal	March 2005
Dieback of Pinus nigra Seedlings Caused by a Strain of Trichoderma viride Li Destri Nicosia, M. G.; Mosca, S.; Mercurio, R. Plant Disease, Vol. 99, Issue 1 https://doi.org/10.1094/PDIS-04-14-0433-RE	journal	January 2015
ClustVis: a web tool for visualizing clustering of multivariate data using Principal Component Analysis and heatmap Metsalu, Tauno; Vilo, Jaak Nucleic Acids Research, Vol. 43, Issue W1 https://doi.org/10.1093/nar/gkv468	journal	May 2015
Improved biocontrol activity of Trichoderma harzianum by over-expression of the proteinase-encoding gene prb1 Flores, A.; Chet, I.; Herrera-Estrella, A. Current Genetics, Vol. 31, Issue 1 https://doi.org/10.1007/s002940050173	journal	January 1997
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
Isolated sinusitis sphenoidalis caused by Trichoderma longibrachiatum in an immunocompetent patient with headache Molnar-Gabor, E.; Doczi, I.; Hatvani, L. Journal of Medical Microbiology, Vol. 62, Issue Pt_8 https://doi.org/10.1099/jmm.0.059485-0	journal	May 2013
Massive Horizontal Gene Transfer in Bdelloid Rotifers Gladyshev, E. A.; Meselson, M.; Arkhipova, I. R. Science, Vol. 320, Issue 5880 https://doi.org/10.1126/science.1156407	journal	May 2008
Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials: A fungal expansin homologue Saloheimo, Markku; Paloheimo, Marja; Hakola, Satu European Journal of Biochemistry, Vol. 269, Issue 17 https://doi.org/10.1046/j.1432-1033.2002.03095.x	journal	August 2002
Tvbgn3, a -1,6-Glucanase from the Biocontrol Fungus Trichoderma virens, Is Involved in Mycoparasitism and Control of Pythium ultimum Djonovic, S.; Pozo, M. J.; Kenerley, C. M. Applied and Environmental Microbiology, Vol. 72, Issue 12 https://doi.org/10.1128/aem.01607-06	journal	September 2006
The Fusarium graminearum Genome Reveals a Link Between Localized Polymorphism and Pathogen Specialization Cuomo, C. A.; Guldener, U.; Xu, J. -R. Science, Vol. 317, Issue 5843 https://doi.org/10.1126/science.1143708	journal	September 2007
AliView: a fast and lightweight alignment viewer and editor for large datasets Larsson, Anders Bioinformatics, Vol. 30, Issue 22 https://doi.org/10.1093/bioinformatics/btu531	journal	August 2014
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
Horizontal gene transfer in eukaryotic algal evolution Raymond, Jason; Blankenship, Robert E. Proceedings of the National Academy of Sciences, Vol. 100, Issue 13 https://doi.org/10.1073/pnas.1533212100	journal	June 2003
Fungal cellulases Wood, Thomas M. Biochemical Society Transactions, Vol. 20, Issue 1 https://doi.org/10.1042/bst0200046	journal	February 1992
Plant Expansins in Bacteria and Fungi: Evolution by Horizontal Gene Transfer and Independent Domain Fusion Nikolaidis, Nikolas; Doran, Nicole; Cosgrove, Daniel J. Molecular Biology and Evolution, Vol. 31, Issue 2 https://doi.org/10.1093/molbev/mst206	journal	October 2013
Accepted Trichoderma names in the year 2015 Bissett, John; Gams, Walter; Jaklitsch, Walter IMA Fungus, Vol. 6, Issue 2 https://doi.org/10.5598/imafungus.2015.06.02.02	journal	September 2015
Draft Genome Sequence of the Cellulolytic Fungus Chaetomium globosum Cuomo, Christina A.; Untereiner, Wendy A.; Ma, Li-Jun Genome Announcements, Vol. 3, Issue 1 https://doi.org/10.1128/genomeA.00021-15	journal	February 2015
PHYML Online--a web server for fast maximum likelihood-based phylogenetic inference Guindon, S.; Lethiec, F.; Duroux, P. Nucleic Acids Research, Vol. 33, Issue Web Server https://doi.org/10.1093/nar/gki352	journal	July 2005
Interkingdom Host Jumping Underground: Phylogenetic Analysis of Entomoparasitic Fungi of the Genus Cordyceps Nikoh, Naruo; Fukatsu, Takema Molecular Biology and Evolution, Vol. 17, Issue 4 https://doi.org/10.1093/oxfordjournals.molbev.a026341	journal	April 2000
Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Tajima, F. Genetics, Vol. 123, Issue 3 https://doi.org/10.1093/genetics/123.3.585	journal	November 1989
Enhanced cellulase production by Trichoderma harzianum by cultivation on glycerol followed by induction on cellulosic substrates da Silva Delabona, Priscila; Lima, Deise Juliana; Robl, Diogo Journal of Industrial Microbiology & Biotechnology, Vol. 43, Issue 5 https://doi.org/10.1007/s10295-016-1744-8	journal	February 2016
ExonHunter: a comprehensive approach to gene finding Brejova, B.; Brown, D. G.; Li, M. Bioinformatics, Vol. 21, Issue Suppl 1 https://doi.org/10.1093/bioinformatics/bti1040	journal	June 2005
The G protein α subunit Tga1 of Trichoderma atroviride is involved in chitinase formation and differential production of antifungal metabolites Reithner, Barbara; Brunner, Kurt; Schuhmacher, Rainer Fungal Genetics and Biology, Vol. 42, Issue 9 https://doi.org/10.1016/j.fgb.2005.04.009	journal	September 2005
Species identification, phylogenetic analysis and detection of herbicide-resistant biotypes of Amaranthus based on ALS and ITS Xu, Han; Pan, Xubin; Wang, Cong Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-68541-x	journal	July 2020
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
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
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
Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans Archibald, J. M.; Rogers, M. B.; Toop, M. Proceedings of the National Academy of Sciences, Vol. 100, Issue 13 https://doi.org/10.1073/pnas.1230951100	journal	May 2003
Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes Richards, T. A.; Soanes, D. M.; Jones, M. D. M. Proceedings of the National Academy of Sciences, Vol. 108, Issue 37 https://doi.org/10.1073/pnas.1105100108	journal	August 2011
Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism Atanasova, Lea; Crom, Stephane Le; Gruber, Sabine BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-121	journal	January 2013
NOTUNG: A Program for Dating Gene Duplications and Optimizing Gene Family Trees Chen, Kevin; Durand, Dannie; Farach-Colton, Martin Journal of Computational Biology, Vol. 7, Issue 3-4 https://doi.org/10.1089/106652700750050871	journal	August 2000
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
Biological control of the root-knot nematode, Meloidogyne incognita on tomato using bioproducts of microbial origin Radwan, M. A.; Farrag, S. A. A.; Abu-Elamayem, M. M. Applied Soil Ecology, Vol. 56 https://doi.org/10.1016/j.apsoil.2012.02.008	journal	May 2012
T-REX: a web server for inferring, validating and visualizing phylogenetic trees and networks Boc, A.; Diallo, A. B.; Makarenkov, V. Nucleic Acids Research, Vol. 40, Issue W1 https://doi.org/10.1093/nar/gks485	journal	June 2012
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DnaSP v5: a software for comprehensive analysis of DNA polymorphism data Librado, P.; Rozas, J. Bioinformatics, Vol. 25, Issue 11 https://doi.org/10.1093/bioinformatics/btp187	journal	April 2009
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Host jumping onto close relatives and across kingdoms by Tyrannicordyceps (Clavicipitaceae) gen. nov. and Ustilaginoidea _(Clavicipitaceae) Kepler, Ryan M.; Sung, Gi-Ho; Harada, Yukio American Journal of Botany, Vol. 99, Issue 3 https://doi.org/10.3732/ajb.1100124	journal	March 2012
Reconciliation with Non-Binary Species Trees Vernot, B.; Stolzer, M.; Goldman, A. Proceedings of the CSB 2007 Conference, Computational Systems Bioinformatics https://doi.org/10.1142/9781860948732_0044	conference	January 2012
Acute Invasive Sinusitis Due to Trichoderma longibrachiatum in a Liver and Small Bowel Transplant Recipient Furukawa, Hiroyuki; Kusne, Shimon; Sutton, Deanna A. Clinical Infectious Diseases, Vol. 26, Issue 2 https://doi.org/10.1086/516317	journal	February 1998
Genomic and transcriptomic analysis of the endophytic fungus Pestalotiopsis fici reveals its lifestyle and high potential for synthesis of natural products Wang, Xiuna; Zhang, Xiaoling; Liu, Ling BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-014-1190-9	journal	January 2015
Chromatin occupancy and target genes of the haematopoietic master transcription factor MYB Lemma, Roza B.; Ledsaak, Marit; Fuglerud, Bettina M. Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-88516-w	journal	April 2021
Plant-symbiotic fungi as chemical engineers: Multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci Schardl, Christopher L.; Young, Carolyn A.; Hesse, Uljana ETH Zurich https://doi.org/10.3929/ethz-b-000073029	text	January 2013
Complete Genome Sequence of Clostridium botulinum CJ0611A1, a Type A(B) Isolate Associated with an International Outbreak of Botulism from Commercial Carrot Juice Harris, Richard; Dussault, Forest; Flint, Annika Microbiology Resource Announcements, Vol. 10, Issue 1 https://doi.org/10.1128/mra.01111-20	journal	January 2021
The Transcription Factor Ste12 Mediates the Regulatory Role of the Tmk1 MAP Kinase in Mycoparasitism and Vegetative Hyphal Fusion in the Filamentous Fungus Trichoderma atroviride Gruber, Sabine; Zeilinger, Susanne PLoS ONE, Vol. 9, Issue 10 https://doi.org/10.1371/journal.pone.0111636	journal	October 2014
Trichoderma atroviride G-Protein α-Subunit Gene tga1 Is Involved in Mycoparasitic Coiling and Conidiation Rocha-Ramírez, Víctor; Omero, Carmi; Chet, Ilan Eukaryotic Cell, Vol. 1, Issue 4 https://doi.org/10.1128/ec.1.4.594-605.2002	journal	August 2002
Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium Ma, Li-Jun; van der Does, H. Charlotte; Borkovich, Katherine A. Nature, Vol. 464, Issue 7287 https://doi.org/10.1038/nature08850	journal	March 2010

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