Comparative Molecular Evolution of Trichoderma Chitinases in Response to Mycoparasitic Interactions

Ihrmark, Katarina; Asmail, Nashwan; Ubhayasekera, Wimal; Melin, Petter; Stenlid, Jan; Karlsson, Magnus

doi:10.4137/ebo.s4198

Comparative Molecular Evolution of Trichoderma Chitinases in Response to Mycoparasitic Interactions

Journal Article · Mon Mar 15 00:00:00 EDT 2010 · Evolutionary Bioinformatics

DOI:https://doi.org/10.4137/ebo.s4198· OSTI ID:1629680

Ihrmark, Katarina ^[1]; Asmail, Nashwan ^[2]; Ubhayasekera, Wimal ^[3]; Melin, Petter ^[4]; Stenlid, Jan ^[2]; Karlsson, Magnus ^[2]

Swedish Univ. of Agricultural Sciences, Uppsala (Sweden). Dept. of Forest Mycology and Pathology; DOE/OSTI
Swedish Univ. of Agricultural Sciences, Uppsala (Sweden). Dept. of Forest Mycology and Pathology
Swedish Univ. of Agricultural Sciences, Uppsala (Sweden). Dept. of Molecular Biology. Biomedical Center; Lund Univ. (Sweden). MAX-lab; Univ. of Copenhagen (Denmark). Inst. of Medicinal Chemistry
Swedish Univ. of Agricultural Sciences, Uppsala (Sweden). Dept. of Microbiology

Certain species of the fungal genus Trichoderma are potent mycoparasites and are used for biological control of fungal diseases on agricultural crops. In Trichoderma, whole-genome sequencing reveal between 20 and 36 different genes encoding chitinases, hydrolytic enzymes that are involved in the mycoparasitic attack. Sequences of Trichoderma chitinase genes chi18-5, chi18-13, chi18-15 and chi18-17, which all exhibit specific expression during mycoparasitism-related conditions, were determined from up to 13 different taxa and studied with regard to their evolutionary patterns. Two of them, chi18-13 and chi18-17, are members of the B1/B2 chitinase subgroup that have expanded significantly in paralog number in mycoparasitic Hypocrea atroviridis and H. virens. Chi18-13 contains two codons that evolve under positive selection and seven groups of co-evolving sites. Chi18-15 displays a unique codon-usage and contains five codons that evolve under positive selection and three groups of co-evolving sites. Regions of high amino acid variability are preferentially localized to substrate- or product side of the catalytic clefts. Differences in amino acid diversity/conservation patterns between different Trichoderma clades are observed. These observations show that Trichoderma chitinases chi18-13 and chi18-15 evolve in a manner consistent with rapid co-evolutionary interactions and identifies putative target regions involved in determining substrate-specificity

View Accepted Manuscript (DOE)

Research Organization:: Swedish University of Agricultural Sciences, Uppsala (Sweden); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning

OSTI ID:: 1629680

Journal Information:: Evolutionary Bioinformatics, Journal Name: Evolutionary Bioinformatics Vol. 6; ISSN 1176-9343

Publisher:: SAGECopyright Statement

Country of Publication:: United States

Language:: English

References (71)

SAM-T04: What is new in protein-structure prediction for CASP6 Karplus, Kevin; Katzman, Sol; Shackleford, George Proteins: Structure, Function, and Bioinformatics, Vol. 61, Issue S7 https://doi.org/10.1002/prot.20730	journal	January 2005
Chitinase Gene Expression during Mycoparasitic Interaction ofTrichoderma harzianumwith Its Host Zeilinger, Susanne; Galhaup, Christiane; Payer, Kathrin Fungal Genetics and Biology, Vol. 26, Issue 2 https://doi.org/10.1006/fgbi.1998.1111	journal	March 1999
A new method for calculating evolutionary substitution rates Lanave, Cecilia; Preparata, Giuliano; Sacone, Cecilia Journal of Molecular Evolution, Vol. 20, Issue 1 https://doi.org/10.1007/bf02101990	journal	February 1984
Expression regulation of the endochitinase chit36 from Trichoderma asperellum ( T. harzianum T-203) Viterbo, Ada; Montero, Manuel; Ramot, Ofir Current Genetics, Vol. 42, Issue 2 https://doi.org/10.1007/s00294-002-0345-4	journal	November 2002
Regulation of chitinase 33 ( chit33 ) gene expression in Trichoderma harzianum de las Mercedes Dana, M.; Limón, M. Carmen; Mejías, Rebeca Current Genetics, Vol. 38, Issue 6 https://doi.org/10.1007/s002940000169	journal	January 2001
The role of an extracellular chitinase from Trichoderma virens Gv29-8 in the biocontrol of Rhizoctonia solani Baek, Jong-Min; Howell, Charles R.; Kenerley, C. M. Current Genetics, Vol. 35, Issue 1 https://doi.org/10.1007/s002940050431	journal	February 1999
Chitinases and Peptide Mimotopes Beauvais, Anne; Latgé, Jean-Paul Chemistry & Biology, Vol. 12, Issue 1 https://doi.org/10.1016/j.chembiol.2005.01.001	journal	January 2005
Structure of Saccharomyces cerevisiae Chitinase 1 and Screening-Based Discovery of Potent Inhibitors Hurtado-Guerrero, Ramon; van Aalten, Daan M. F. Chemistry & Biology, Vol. 14, Issue 5 https://doi.org/10.1016/j.chembiol.2007.03.015	journal	May 2007
An oligonucleotide barcode for species identification in Trichoderma and Hypocrea Druzhinina, Irina S.; Kopchinskiy, Alexei G.; Komoń, Monika Fungal Genetics and Biology, Vol. 42, Issue 10 https://doi.org/10.1016/j.fgb.2005.06.007	journal	October 2005
Natural history and evolutionary principles of gene duplication in fungi Wapinski, Ilan; Pfeffer, Avi; Friedman, Nir Nature, Vol. 449, Issue 7158 https://doi.org/10.1038/nature06107	journal	September 2007
Trichoderma species — opportunistic, avirulent plant symbionts Harman, Gary E.; Howell, Charles R.; Viterbo, Ada Nature Reviews Microbiology, Vol. 2, Issue 1 https://doi.org/10.1038/nrmicro797	journal	January 2004
Characterization of ech-42, a Trichoderma harzianum endochitinase gene expressed during mycoparasitism. Carsolio, C.; Gutiérrez, A.; Jiménez, B. Proceedings of the National Academy of Sciences, Vol. 91, Issue 23 https://doi.org/10.1073/pnas.91.23.10903	journal	November 1994
InterProScan - an integration platform for the signature-recognition methods in InterPro Zdobnov, E. M.; Apweiler, R. Bioinformatics, Vol. 17, Issue 9, p. 847-848 https://doi.org/10.1093/bioinformatics/17.9.847	journal	September 2001
Rate4Site: an algorithmic tool for the identification of functional regions in proteins by surface mapping of evolutionary determinants within their homologues Pupko, T.; Bell, R. E.; Mayrose, I. Bioinformatics, Vol. 18, Issue Suppl 1 https://doi.org/10.1093/bioinformatics/18.suppl_1.s71	journal	July 2002
The rapid generation of mutation data matrices from protein sequences Jones, David T.; Taylor, William R.; Thornton, Janet M. Bioinformatics, Vol. 8, Issue 3 https://doi.org/10.1093/bioinformatics/8.3.275	journal	January 1992
HyPhy: hypothesis testing using phylogenies Pond, S. L. K.; Frost, S. D. W.; Muse, S. V. Bioinformatics, Vol. 21, Issue 5 https://doi.org/10.1093/bioinformatics/bti079	journal	October 2004
Datamonkey: rapid detection of selective pressure on individual sites of codon alignments Pond, S. L. K.; Frost, S. D. W. Bioinformatics, Vol. 21, Issue 10 https://doi.org/10.1093/bioinformatics/bti320	journal	February 2005
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
Differential recognition of animal type 4-galactosylated and 3-fucosylated chito-oligosaccharides by two family 18 chitinases from Trichoderma harzianum Boer, H. Glycobiology, Vol. 14, Issue 12 https://doi.org/10.1093/glycob/cwh121	journal	July 2004
A Simple Hierarchical Approach to Modeling Distributions of Substitution Rates Kosakovsky Pond, Sergei L.; Frost, Simon D. W. Molecular Biology and Evolution, Vol. 22, Issue 2 https://doi.org/10.1093/molbev/msi009	journal	October 2004
Not So Different After All: A Comparison of Methods for Detecting Amino Acid Sites Under Selection Kosakovsky Pond, Sergei L.; Frost, Simon D. W. Molecular Biology and Evolution, Vol. 22, Issue 5 https://doi.org/10.1093/molbev/msi105	journal	February 2005
MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0 Tamura, K.; Dudley, J.; Nei, M. Molecular Biology and Evolution, Vol. 24, Issue 8 https://doi.org/10.1093/molbev/msm092	journal	April 2007
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
The Protein Data Bank Berman, H. M. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.235	journal	January 2000
CDD: a Conserved Domain Database for protein classification Marchler-Bauer, A. Nucleic Acids Research, Vol. 33, Issue Database issue https://doi.org/10.1093/nar/gki069	journal	December 2004
GenBank Benson, D. A.; Karsch-Mizrachi, I.; Lipman, D. J. Nucleic Acids Research, Vol. 36, Issue Database https://doi.org/10.1093/nar/gkm929	journal	December 2007
Differential Expression ofTrichoderma harzianumChitinases During Mycoparasitism Haran, S. Phytopathology, Vol. 86, Issue 9 https://doi.org/10.1094/phyto-86-980	journal	January 1996
MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures Kraulis, P. J. Journal of Applied Crystallography, Vol. 24, Issue 5 https://doi.org/10.1107/s0021889891004399	journal	October 1991
Improved methods for building protein models in electron density maps and the location of errors in these models Jones, T. A.; Zou, J. Y.; Cowan, S. W. Acta Crystallographica Section A Foundations of Crystallography, Vol. 47, Issue 2, p. 110-119 https://doi.org/10.1107/s0108767390010224	journal	March 1991
Molray – a web interface between O and the POV-Ray ray tracer Harris, Mark; Jones, T. Alwyn Acta Crystallographica Section D Biological Crystallography, Vol. 57, Issue 8 https://doi.org/10.1107/s0907444901007697	journal	July 2001
ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts Gardes, M.; Bruns, T. D. Molecular Ecology, Vol. 2, Issue 2 https://doi.org/10.1111/j.1365-294x.1993.tb00005.x	journal	April 1993
Isolation and characterization of three chitinases from Trichoderma harzianum Cruz, Jesus; Hidalgo-Gallego, Antonio; Lora, Jose M. European Journal of Biochemistry, Vol. 206, Issue 3 https://doi.org/10.1111/j.1432-1033.1992.tb16994.x	journal	June 1992
Addition of substrate-binding domains increases substrate-binding capacity and specific activity of a chitinase fromTrichoderma harzianum LimÃ³n, M. Carmen; Margolles-Clark, Emilio; BenÄ±Ìtez, TahÄ±Ìa FEMS Microbiology Letters, Vol. 198, Issue 1 https://doi.org/10.1111/j.1574-6968.2001.tb10619.x	journal	April 2001
Parallel formation and synergism of hydrolytic enzymes and peptaibol antibiotics, molecular mechanisms involved in the antagonistic action of Trichoderma harzianum against phytopathogenic fungi. Schirmböck, M.; Lorito, M.; Wang, Y. L. Applied and Environmental Microbiology, Vol. 60, Issue 12 https://doi.org/10.1128/aem.60.12.4364-4370.1994	journal	January 1994
Role of the Trichoderma harzianum Endochitinase Gene, ech42 , in Mycoparasitism Carsolio, Carolina; Benhamou, Nicole; Haran, Shoshan Applied and Environmental Microbiology, Vol. 65, Issue 3 https://doi.org/10.1128/aem.65.3.929-935.1999	journal	March 1999
Evolution of Family 18 Glycoside Hydrolases: Diversity, Domain Structures and Phylogenetic Relationships Karlsson, Magnus; Stenlid, Jan Microbial Physiology, Vol. 16, Issue 3-4 https://doi.org/10.1159/000151220	journal	August 2008
Comparative Evolutionary Histories of Chitinase Genes in the Genus Zea and Family PoaceaeSequence data from this article have been deposited with the EMBL/GenBank Data Libraries under accession nos. AY532721, AY532722, AY532723, AY532724, AY532725, AY532726, AY532727, AY532728, AY532729, AY532730, AY532731, AY532732, AY532733, AY532734, AY532735, AY532736, AY532737, AY532738, AY532739, AY532740, AY532741, AY532742, AY532743, AY532744, AY532745, AY532746, AY532747, AY532748, AY532749, AY532750, AY532751, AY532752, AY532753, AY532754, AY532755, AY532756, AY532757, AY532758, AY532759, AY532760, AY532761, AY532762, AY532763, AY532764, AY532765, AY532766, AY532767, AY532768, AY532769, AY532770, AY532771, AY532772, AY532773, AY532774, AY532775, AY532776, AY532777, AY532778, AY532779, AY532780, AY532781, AY532782, AY532783, AY532784, AY532785, AY532786, AY532787, AY532788. Tiffin, Peter Genetics, Vol. 167, Issue 3 https://doi.org/10.1534/genetics.104.026856	journal	July 2004
Species concepts and biodiversity in Trichoderma and Hypocrea : from aggregate species to species clusters? Druzhinina, Irina; Kubicek, Christian P. Journal of Zhejiang University SCIENCE, Vol. 6B, Issue 2 https://doi.org/10.1631/jzus.2005.b0100	journal	January 2005
Comparative Evolutionary Histories of the Fungal Chitinase Gene Family Reveal Non-Random Size Expansions and Contractions due to Adaptive Natural Selection Karlsson, Magnus; Stenlid, Jan Evolutionary Bioinformatics, Vol. 4 https://doi.org/10.4137/ebo.s604	journal	January 2008
Cloning and characterization of a chitinase (CHIT42) cDNA from the mycoparasitic fungus Trichoderma harzianum García, Irene; Lora, José M.; de la Cruz, Jesús Current Genetics, Vol. 27, Issue 1 https://doi.org/10.1007/BF00326583	journal	December 1994
Trichoderma hamatum: Its hyphal interactions withRhizoctonia solani andPythium spp. Chet, I.; Harman, G. E.; Baker, R. Microbial Ecology, Vol. 7, Issue 1 https://doi.org/10.1007/BF02010476	journal	March 1981
A new method for calculating evolutionary substitution rates Lanave, Cecilia; Preparata, Giuliano; Sacone, Cecilia Journal of Molecular Evolution, Vol. 20, Issue 1 https://doi.org/10.1007/BF02101990	journal	February 1984
Cloning and characterization of multiple glycosyl hydrolase genes from Trichoderma virens Kim, Dong-Jin; Baek, Jong-Min; Uribe, Pedro Current Genetics, Vol. 40, Issue 6 https://doi.org/10.1007/s00294-001-0267-6	journal	March 2002
Review of Fungal Chitinases Duo-Chuan, Li Mycopathologia, Vol. 161, Issue 6 https://doi.org/10.1007/s11046-006-0024-y	journal	June 2006
The general stochastic model of nucleotide substitution Rodríguez, F.; Oliver, J. L.; Marín, A. Journal of Theoretical Biology, Vol. 142, Issue 4 https://doi.org/10.1016/S0022-5193(05)80104-3	journal	February 1990
Addition of substrate-binding domains increases substrate-binding capacity and specific activity of a chitinase from Trichoderma harzianum Limón, M. FEMS Microbiology Letters, Vol. 198, Issue 1 https://doi.org/10.1016/S0378-1097(01)00124-0	journal	April 2001
Overexpression and characterization of a novel chitinase from Trichoderma atroviride strain P1 Hoell, Ingunn A.; Klemsdal, Sonja S.; Vaaje-Kolstad, Gustav Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1748, Issue 2 https://doi.org/10.1016/j.bbapap.2005.01.002	journal	May 2005
Specificity and Affinity of Natural Product Cyclopentapeptide Inhibitors against A. fumigatus, Human, and Bacterial Chitinases Rao, Francesco V.; Houston, Douglas R.; Boot, Rolf G. Chemistry & Biology, Vol. 12, Issue 1 https://doi.org/10.1016/j.chembiol.2004.10.013	journal	January 2005
Chitinases of filamentous fungi: a large group of diverse proteins with multiple physiological functions Seidl, Verena Fungal Biology Reviews, Vol. 22, Issue 1 https://doi.org/10.1016/j.fbr.2008.03.002	journal	February 2008
Rapid evolution in plant chitinases: Molecular targets of selection in plant-pathogen coevolution Bishop, J. G.; Dean, A. M.; Mitchell-Olds, T. Proceedings of the National Academy of Sciences, Vol. 97, Issue 10 https://doi.org/10.1073/pnas.97.10.5322	journal	May 2000
Rate4Site: an algorithmic tool for the identification of functional regions in proteins by surface mapping of evolutionary determinants within their homologues Pupko, T.; Bell, R. E.; Mayrose, I. Bioinformatics, Vol. 18, Issue Suppl 1 https://doi.org/10.1093/bioinformatics/18.suppl_1.S71	journal	July 2002
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
Comparison of Site-Specific Rate-Inference Methods for Protein Sequences: Empirical Bayesian Methods Are Superior Mayrose, I. Molecular Biology and Evolution, Vol. 21, Issue 9 https://doi.org/10.1093/molbev/msh194	journal	May 2004
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Thompson, Julie D.; Higgins, Desmond G.; Gibson, Toby J. Nucleic Acids Research, Vol. 22, Issue 22, p. 4673-4680 https://doi.org/10.1093/nar/22.22.4673	journal	January 1994
Disruption of the ech42 (Endochitinase-Encoding) Gene Affects Biocontrol Activity in Trichoderma harzianum P1 Woo, S. L.; Donzelli, B.; Scala, F. Molecular Plant-Microbe Interactions®, Vol. 12, Issue 5 https://doi.org/10.1094/MPMI.1999.12.5.419	journal	May 1999
Mechanisms Employed by Trichoderma Species in the Biological Control of Plant Diseases: The History and Evolution of Current Concepts Howell, C. R. Plant Disease, Vol. 87, Issue 1 https://doi.org/10.1094/PDIS.2003.87.1.4	journal	January 2003
Differential Expression ofTrichoderma harzianumChitinases During Mycoparasitism Haran, S. Phytopathology, Vol. 86, Issue 9 https://doi.org/10.1094/Phyto-86-980	journal	January 1996
Estimating the tempo and mode of gene family evolution from comparative genomic data Hahn, M. W. Genome Research, Vol. 15, Issue 8 https://doi.org/10.1101/gr.3567505	journal	August 2005
MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures Kraulis, P. J. Journal of Applied Crystallography, Vol. 24, Issue 5 https://doi.org/10.1107/S0021889891004399	journal	October 1991
Improved methods for building protein models in electron density maps and the location of errors in these models Jones, T. A.; Zou, J. Y.; Cowan, S. W. Acta Crystallographica Section A Foundations of Crystallography, Vol. 47, Issue 2, p. 110-119 https://doi.org/10.1107/S0108767390010224	journal	March 1991
Molray – a web interface between O and the POV-Ray ray tracer Harris, Mark; Jones, T. Alwyn Acta Crystallographica Section D Biological Crystallography, Vol. 57, Issue 8 https://doi.org/10.1107/S0907444901007697	journal	July 2001
ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts Gardes, M.; Bruns, T. D. Molecular Ecology, Vol. 2, Issue 2 https://doi.org/10.1111/j.1365-294X.1993.tb00005.x	journal	April 1993
Molecular cloning, characterization, and expression studies of a novel chitinase gene (ech30) from the mycoparasite Trichoderma atroviride strain P1 Klemsdal, Sonja S.; Clarke, Jihong Liu; Hoell, Ingunn A. FEMS Microbiology Letters, Vol. 256, Issue 2 https://doi.org/10.1111/j.1574-6968.2006.00132.x	journal	March 2006
A complete survey of Trichoderma chitinases reveals three distinct subgroups of family 18 chitinases: Trichoderma chitinases Seidl, Verena; Huemer, Birgit; Seiboth, Bernhard FEBS Journal, Vol. 272, Issue 22 https://doi.org/10.1111/j.1742-4658.2005.04994.x	journal	November 2005
cDNA cloning and 1.75 Å crystal structure determination of PPL2, an endochitinase and N-acetylglucosamine-binding hemagglutinin from Parkia platycephala seeds Cavada, Benildo S.; Moreno, Frederico B. B.; Da Rocha, Bruno A. M. FEBS Journal, Vol. 273, Issue 17 https://doi.org/10.1111/j.1742-4658.2006.05400.x	journal	July 2006
Parallel formation and synergism of hydrolytic enzymes and peptaibol antibiotics, molecular mechanisms involved in the antagonistic action of Trichoderma harzianum against phytopathogenic fungi. Schirmböck, M.; Lorito, M.; Wang, Y. L. Applied and Environmental Microbiology, Vol. 60, Issue 12 https://doi.org/10.1128/AEM.60.12.4364-4370.1994	journal	January 1994
Role of the Trichoderma harzianum Endochitinase Gene, ech42 , in Mycoparasitism Carsolio, Carolina; Benhamou, Nicole; Haran, Shoshan Applied and Environmental Microbiology, Vol. 65, Issue 3 https://doi.org/10.1128/AEM.65.3.929-935.1999	journal	March 1999
Expression of Two Major Chitinase Genes of Trichoderma atroviride ( T. harzianum P1) Is Triggered by Different Regulatory Signals Mach, Robert L.; Peterbauer, Clemens K.; Payer, Kathrin Applied and Environmental Microbiology, Vol. 65, Issue 5 https://doi.org/10.1128/AEM.65.5.1858-1863.1999	journal	May 1999
An Evolutionary-Network Model Reveals Stratified Interactions in the V3 Loop of the HIV-1 Envelope Poon, Art F. Y.; Lewis, Fraser I.; Pond, Sergei L. Kosakovsky PLoS Computational Biology, Vol. 3, Issue 11 https://doi.org/10.1371/journal.pcbi.0030231	journal	November 2007
Species concepts and biodiversity in Trichoderma and Hypocrea : from aggregate species to species clusters? Druzhinina, Irina; Kubicek, Christian P. Journal of Zhejiang University SCIENCE, Vol. 6B, Issue 2 https://doi.org/10.1631/jzus.2005.B0100	journal	January 2005
Reverse Conservation Analysis Reveals the Specificity Determining Residues of Cytochrome P450 Family 2 (CYP 2) Lee, Tai-Sung Evolutionary Bioinformatics, Vol. 4 https://doi.org/10.4137/EBO.S291	journal	January 2008

Cited By (11)

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
Insights on the Evolution of Mycoparasitism from the Genome of Clonostachys rosea Karlsson, Magnus; Durling, Mikael Brandström; Choi, Jaeyoung Genome Biology and Evolution, Vol. 7, Issue 2 https://doi.org/10.1093/gbe/evu292	journal	January 2015
Genome Sequence, Comparative Analysis, and Evolutionary Insights into Chitinases of Entomopathogenic Fungus Hirsutella thompsonii Agrawal, Yamini; Khatri, Indu; Subramanian, Srikrishna Genome Biology and Evolution, Vol. 7, Issue 3 https://doi.org/10.1093/gbe/evv037	journal	February 2015
Bacterial and fungal chitinase chiJ orthologs evolve under different selective constraints following horizontal gene transfer Ubhayasekera, Wimal; Karlsson, Magnus BMC Research Notes, Vol. 5, Issue 1 https://doi.org/10.1186/1756-0500-5-581	journal	October 2012
Disruption of the Eng18B ENGase Gene in the Fungal Biocontrol Agent Trichoderma atroviride Affects Growth, Conidiation and Antagonistic Ability Dubey, Mukesh K.; Ubhayasekera, Wimal; Sandgren, Mats PLoS ONE, Vol. 7, Issue 5 https://doi.org/10.1371/journal.pone.0036152	journal	May 2012
Encapsulation of Trichoderma harzianum Preserves Enzymatic Activity and Enhances the Potential for Biological Control Maruyama, Cintia Rodrigues; Bilesky-José, Natália; de Lima, Renata Frontiers in Bioengineering and Biotechnology, Vol. 8 https://doi.org/10.3389/fbioe.2020.00225	journal	March 2020
Integrated Translatome and Proteome: Approach for Accurate Portraying of Widespread Multifunctional Aspects of Trichoderma Sharma, Vivek; Salwan, Richa; Sharma, P. N. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01602	journal	August 2017
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
Identifying glycoside hydrolase family 18 genes in the mycoparasitic fungal species Clonostachys rosea Karlsson, Magnus; Jensen, Dan Funck; Dubey, Mukesh Microbiology, Vol. 161, Issue 7 https://doi.org/10.1099/mic.0.000096	journal	July 2015
Chitinolytic assay of indigenous Trichoderma isolates collected from different geographical locations of Chhattisgarh in Central India Agrawal, Toshy; Kotasthane, Anil S. SpringerPlus, Vol. 1, Issue 1 https://doi.org/10.1186/2193-1801-1-73	journal	December 2012
Paleozoic diversification of terrestrial chitin-degrading bacterial lineages Gruen, Danielle S.; Wolfe, Joanna M.; Fournier, Gregory P. BMC Evolutionary Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s12862-019-1357-8	journal	January 2019

Similar Records

Evolution and comparative genomics of the most common Trichoderma species

Journal Article · Wed Jun 12 00:00:00 EDT 2019 · BMC Genomics · OSTI ID:1619122

Transcriptomic response of the mycoparasitic fungus Trichoderma atroviride to the presence of a fungal prey

Journal Article · Fri Jul 23 00:00:00 EDT 2010 · BMC Genomics · OSTI ID:985907

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Trichodema
chitinase
mycoparasitism
protein evolution

Comparative Molecular Evolution of Trichoderma Chitinases in Response to Mycoparasitic Interactions

Citation Formats

References (71)

Cited By (11)

Similar Records

Related Subjects