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Title: Comparative Molecular Evolution of Trichoderma Chitinases in Response to Mycoparasitic Interactions

Abstract

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

Authors:
 [1];  [1];  [2];  [3];  [1];  [1]
  1. Swedish Univ. of Agricultural Sciences, Uppsala (Sweden). Dept. of Forest Mycology and Pathology
  2. 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
  3. Swedish Univ. of Agricultural Sciences, Uppsala (Sweden). Dept. of Microbiology
Publication Date:
Research Org.:
Swedish Univ. of Agricultural Sciences, Uppsala (Sweden); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Sponsoring Org.:
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 Identifier:
1629680
Resource Type:
Accepted Manuscript
Journal Name:
Evolutionary Bioinformatics
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 1176-9343
Publisher:
SAGE
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; protein evolution; Trichodema; mycoparasitism; chitinase

Citation Formats

Ihrmark, Katarina, Asmail, Nashwan, Ubhayasekera, Wimal, Melin, Petter, Stenlid, Jan, and Karlsson, Magnus. Comparative Molecular Evolution of Trichoderma Chitinases in Response to Mycoparasitic Interactions. United States: N. p., 2010. Web. doi:10.4137/ebo.s4198.
Ihrmark, Katarina, Asmail, Nashwan, Ubhayasekera, Wimal, Melin, Petter, Stenlid, Jan, & Karlsson, Magnus. Comparative Molecular Evolution of Trichoderma Chitinases in Response to Mycoparasitic Interactions. United States. https://doi.org/10.4137/ebo.s4198
Ihrmark, Katarina, Asmail, Nashwan, Ubhayasekera, Wimal, Melin, Petter, Stenlid, Jan, and Karlsson, Magnus. Mon . "Comparative Molecular Evolution of Trichoderma Chitinases in Response to Mycoparasitic Interactions". United States. https://doi.org/10.4137/ebo.s4198. https://www.osti.gov/servlets/purl/1629680.
@article{osti_1629680,
title = {Comparative Molecular Evolution of Trichoderma Chitinases in Response to Mycoparasitic Interactions},
author = {Ihrmark, Katarina and Asmail, Nashwan and Ubhayasekera, Wimal and Melin, Petter and Stenlid, Jan and Karlsson, Magnus},
abstractNote = {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},
doi = {10.4137/ebo.s4198},
journal = {Evolutionary Bioinformatics},
number = ,
volume = 6,
place = {United States},
year = {Mon Mar 15 00:00:00 EDT 2010},
month = {Mon Mar 15 00:00:00 EDT 2010}
}

Works referenced in this record:

GenBank
journal, December 2007

  • Benson, D. A.; Karsch-Mizrachi, I.; Lipman, D. J.
  • Nucleic Acids Research, Vol. 36, Issue Database
  • DOI: 10.1093/nar/gkm929

A Simple Hierarchical Approach to Modeling Distributions of Substitution Rates
journal, October 2004

  • Kosakovsky Pond, Sergei L.; Frost, Simon D. W.
  • Molecular Biology and Evolution, Vol. 22, Issue 2
  • DOI: 10.1093/molbev/msi009

Chitinase Gene Expression during Mycoparasitic Interaction ofTrichoderma harzianumwith Its Host
journal, March 1999

  • Zeilinger, Susanne; Galhaup, Christiane; Payer, Kathrin
  • Fungal Genetics and Biology, Vol. 26, Issue 2
  • DOI: 10.1006/fgbi.1998.1111

An oligonucleotide barcode for species identification in Trichoderma and Hypocrea
journal, October 2005

  • Druzhinina, Irina S.; Kopchinskiy, Alexei G.; Komoń, Monika
  • Fungal Genetics and Biology, Vol. 42, Issue 10
  • DOI: 10.1016/j.fgb.2005.06.007

Molray – a web interface between O and the POV-Ray ray tracer
journal, July 2001

  • Harris, Mark; Jones, T. Alwyn
  • Acta Crystallographica Section D Biological Crystallography, Vol. 57, Issue 8
  • DOI: 10.1107/s0907444901007697

Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
journal, September 1997

  • Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A.
  • Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402
  • DOI: 10.1093/nar/25.17.3389

A new method for calculating evolutionary substitution rates
journal, February 1984

  • Lanave, Cecilia; Preparata, Giuliano; Sacone, Cecilia
  • Journal of Molecular Evolution, Vol. 20, Issue 1
  • DOI: 10.1007/bf02101990

The Protein Data Bank
journal, January 2000


InterProScan - an integration platform for the signature-recognition methods in InterPro
journal, September 2001


Regulation of chitinase 33 ( chit33 ) gene expression in Trichoderma harzianum
journal, January 2001

  • de las Mercedes Dana, M.; Limón, M. Carmen; Mejías, Rebeca
  • Current Genetics, Vol. 38, Issue 6
  • DOI: 10.1007/s002940000169

Chitinases and Peptide Mimotopes
journal, January 2005


Datamonkey: rapid detection of selective pressure on individual sites of codon alignments
journal, February 2005


MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures
journal, October 1991


Evolution of Family 18 Glycoside Hydrolases: Diversity, Domain Structures and Phylogenetic Relationships
journal, August 2008

  • Karlsson, Magnus; Stenlid, Jan
  • Microbial Physiology, Vol. 16, Issue 3-4
  • DOI: 10.1159/000151220

Clustal W and Clustal X version 2.0
journal, September 2007


MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0
journal, April 2007

  • Tamura, K.; Dudley, J.; Nei, M.
  • Molecular Biology and Evolution, Vol. 24, Issue 8
  • DOI: 10.1093/molbev/msm092

Improved methods for building protein models in electron density maps and the location of errors in these models
journal, March 1991

  • Jones, T. A.; Zou, J. Y.; Cowan, S. W.
  • Acta Crystallographica Section A Foundations of Crystallography, Vol. 47, Issue 2, p. 110-119
  • DOI: 10.1107/s0108767390010224

SAM-T04: What is new in protein-structure prediction for CASP6
journal, January 2005

  • Karplus, Kevin; Katzman, Sol; Shackleford, George
  • Proteins: Structure, Function, and Bioinformatics, Vol. 61, Issue S7
  • DOI: 10.1002/prot.20730

Isolation and characterization of three chitinases from Trichoderma harzianum
journal, June 1992


Addition of substrate-binding domains increases substrate-binding capacity and specific activity of a chitinase fromTrichoderma harzianum
journal, April 2001


Not So Different After All: A Comparison of Methods for Detecting Amino Acid Sites Under Selection
journal, February 2005

  • Kosakovsky Pond, Sergei L.; Frost, Simon D. W.
  • Molecular Biology and Evolution, Vol. 22, Issue 5
  • DOI: 10.1093/molbev/msi105

CDD: a Conserved Domain Database for protein classification
journal, December 2004

  • Marchler-Bauer, A.
  • Nucleic Acids Research, Vol. 33, Issue Database issue
  • DOI: 10.1093/nar/gki069

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.
journal, July 2004


Characterization of ech-42, a Trichoderma harzianum endochitinase gene expressed during mycoparasitism.
journal, November 1994

  • Carsolio, C.; Gutiérrez, A.; Jiménez, B.
  • Proceedings of the National Academy of Sciences, Vol. 91, Issue 23
  • DOI: 10.1073/pnas.91.23.10903

The rapid generation of mutation data matrices from protein sequences
journal, January 1992


Expression regulation of the endochitinase chit36 from Trichoderma asperellum ( T. harzianum T-203)
journal, November 2002


HyPhy: hypothesis testing using phylogenies
journal, October 2004


The role of an extracellular chitinase from Trichoderma virens Gv29-8 in the biocontrol of Rhizoctonia solani
journal, February 1999

  • Baek, Jong-Min; Howell, Charles R.; Kenerley, C. M.
  • Current Genetics, Vol. 35, Issue 1
  • DOI: 10.1007/s002940050431

Differential Expression ofTrichoderma harzianumChitinases During Mycoparasitism
journal, January 1996


Natural history and evolutionary principles of gene duplication in fungi
journal, September 2007

  • Wapinski, Ilan; Pfeffer, Avi; Friedman, Nir
  • Nature, Vol. 449, Issue 7158
  • DOI: 10.1038/nature06107

Species concepts and biodiversity in Trichoderma and Hypocrea : from aggregate species to species clusters?
journal, January 2005

  • Druzhinina, Irina; Kubicek, Christian P.
  • Journal of Zhejiang University SCIENCE, Vol. 6B, Issue 2
  • DOI: 10.1631/jzus.2005.b0100

Role of the Trichoderma harzianum Endochitinase Gene, ech42 , in Mycoparasitism
journal, March 1999

  • Carsolio, Carolina; Benhamou, Nicole; Haran, Shoshan
  • Applied and Environmental Microbiology, Vol. 65, Issue 3
  • DOI: 10.1128/aem.65.3.929-935.1999

Trichoderma species — opportunistic, avirulent plant symbionts
journal, January 2004

  • Harman, Gary E.; Howell, Charles R.; Viterbo, Ada
  • Nature Reviews Microbiology, Vol. 2, Issue 1
  • DOI: 10.1038/nrmicro797

Structure of Saccharomyces cerevisiae Chitinase 1 and Screening-Based Discovery of Potent Inhibitors
journal, May 2007


Trichoderma species — opportunistic, avirulent plant symbionts
journal, January 2004

  • Harman, Gary E.; Howell, Charles R.; Viterbo, Ada
  • Nature Reviews Microbiology, Vol. 2, Issue 1
  • DOI: 10.1038/nrmicro797

Trichoderma hamatum: Its hyphal interactions withRhizoctonia solani andPythium spp.
journal, March 1981

  • Chet, I.; Harman, G. E.; Baker, R.
  • Microbial Ecology, Vol. 7, Issue 1
  • DOI: 10.1007/BF02010476

Review of Fungal Chitinases
journal, June 2006


Chitinases of filamentous fungi: a large group of diverse proteins with multiple physiological functions
journal, February 2008


A complete survey of Trichoderma chitinases reveals three distinct subgroups of family 18 chitinases: Trichoderma chitinases
journal, November 2005


Evolution of Family 18 Glycoside Hydrolases: Diversity, Domain Structures and Phylogenetic Relationships
journal, August 2008

  • Karlsson, Magnus; Stenlid, Jan
  • Microbial Physiology, Vol. 16, Issue 3-4
  • DOI: 10.1159/000151220

Molecular cloning, characterization, and expression studies of a novel chitinase gene (ech30) from the mycoparasite Trichoderma atroviride strain P1
journal, March 2006


Cloning and characterization of multiple glycosyl hydrolase genes from Trichoderma virens
journal, March 2002


Expression regulation of the endochitinase chit36 from Trichoderma asperellum ( T. harzianum T-203)
journal, November 2002


Regulation of chitinase 33 ( chit33 ) gene expression in Trichoderma harzianum
journal, January 2001

  • de las Mercedes Dana, M.; Limón, M. Carmen; Mejías, Rebeca
  • Current Genetics, Vol. 38, Issue 6
  • DOI: 10.1007/s002940000169

Chitinase Gene Expression during Mycoparasitic Interaction ofTrichoderma harzianumwith Its Host
journal, March 1999

  • Zeilinger, Susanne; Galhaup, Christiane; Payer, Kathrin
  • Fungal Genetics and Biology, Vol. 26, Issue 2
  • DOI: 10.1006/fgbi.1998.1111

Rapid evolution in plant chitinases: Molecular targets of selection in plant-pathogen coevolution
journal, May 2000

  • Bishop, J. G.; Dean, A. M.; Mitchell-Olds, T.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 10
  • DOI: 10.1073/pnas.97.10.5322

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.
journal, July 2004


An oligonucleotide barcode for species identification in Trichoderma and Hypocrea
journal, October 2005

  • Druzhinina, Irina S.; Kopchinskiy, Alexei G.; Komoń, Monika
  • Fungal Genetics and Biology, Vol. 42, Issue 10
  • DOI: 10.1016/j.fgb.2005.06.007

CAFE: a computational tool for the study of gene family evolution
journal, March 2006


Estimating the tempo and mode of gene family evolution from comparative genomic data
journal, August 2005


Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
journal, September 1997

  • Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A.
  • Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402
  • DOI: 10.1093/nar/25.17.3389

InterProScan - an integration platform for the signature-recognition methods in InterPro
journal, September 2001


CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice
journal, January 1994

  • Thompson, Julie D.; Higgins, Desmond G.; Gibson, Toby J.
  • Nucleic Acids Research, Vol. 22, Issue 22, p. 4673-4680
  • DOI: 10.1093/nar/22.22.4673

MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0
journal, April 2007

  • Tamura, K.; Dudley, J.; Nei, M.
  • Molecular Biology and Evolution, Vol. 24, Issue 8
  • DOI: 10.1093/molbev/msm092

Clustal W and Clustal X version 2.0
journal, September 2007


GenBank
journal, December 2007

  • Benson, D. A.; Karsch-Mizrachi, I.; Lipman, D. J.
  • Nucleic Acids Research, Vol. 36, Issue Database
  • DOI: 10.1093/nar/gkm929

SAM-T04: What is new in protein-structure prediction for CASP6
journal, January 2005

  • Karplus, Kevin; Katzman, Sol; Shackleford, George
  • Proteins: Structure, Function, and Bioinformatics, Vol. 61, Issue S7
  • DOI: 10.1002/prot.20730

The Protein Data Bank
journal, January 2000


Specificity and Affinity of Natural Product Cyclopentapeptide Inhibitors against A. fumigatus, Human, and Bacterial Chitinases
journal, January 2005


Structure of Saccharomyces cerevisiae Chitinase 1 and Screening-Based Discovery of Potent Inhibitors
journal, May 2007


Not So Different After All: A Comparison of Methods for Detecting Amino Acid Sites Under Selection
journal, February 2005

  • Kosakovsky Pond, Sergei L.; Frost, Simon D. W.
  • Molecular Biology and Evolution, Vol. 22, Issue 5
  • DOI: 10.1093/molbev/msi105

HyPhy: hypothesis testing using phylogenies
journal, October 2004


Datamonkey: rapid detection of selective pressure on individual sites of codon alignments
journal, February 2005


A Simple Hierarchical Approach to Modeling Distributions of Substitution Rates
journal, October 2004

  • Kosakovsky Pond, Sergei L.; Frost, Simon D. W.
  • Molecular Biology and Evolution, Vol. 22, Issue 2
  • DOI: 10.1093/molbev/msi009

An Evolutionary-Network Model Reveals Stratified Interactions in the V3 Loop of the HIV-1 Envelope
journal, November 2007

  • Poon, Art F. Y.; Lewis, Fraser I.; Pond, Sergei L. Kosakovsky
  • PLoS Computational Biology, Vol. 3, Issue 11
  • DOI: 10.1371/journal.pcbi.0030231

CDD: a Conserved Domain Database for protein classification
journal, December 2004

  • Marchler-Bauer, A.
  • Nucleic Acids Research, Vol. 33, Issue Database issue
  • DOI: 10.1093/nar/gki069

Natural history and evolutionary principles of gene duplication in fungi
journal, September 2007

  • Wapinski, Ilan; Pfeffer, Avi; Friedman, Nir
  • Nature, Vol. 449, Issue 7158
  • DOI: 10.1038/nature06107

Overexpression and characterization of a novel chitinase from Trichoderma atroviride strain P1
journal, May 2005

  • Hoell, Ingunn A.; Klemsdal, Sonja S.; Vaaje-Kolstad, Gustav
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1748, Issue 2
  • DOI: 10.1016/j.bbapap.2005.01.002

Isolation and characterization of three chitinases from Trichoderma harzianum
journal, June 1992


Characterization of ech-42, a Trichoderma harzianum endochitinase gene expressed during mycoparasitism.
journal, November 1994

  • Carsolio, C.; Gutiérrez, A.; Jiménez, B.
  • Proceedings of the National Academy of Sciences, Vol. 91, Issue 23
  • DOI: 10.1073/pnas.91.23.10903

Cloning and characterization of a chitinase (CHIT42) cDNA from the mycoparasitic fungus Trichoderma harzianum
journal, December 1994

  • García, Irene; Lora, José M.; de la Cruz, Jesús
  • Current Genetics, Vol. 27, Issue 1
  • DOI: 10.1007/BF00326583

Expression of Two Major Chitinase Genes of Trichoderma atroviride ( T. harzianum P1) Is Triggered by Different Regulatory Signals
journal, May 1999


Disruption of the ech42 (Endochitinase-Encoding) Gene Affects Biocontrol Activity in Trichoderma harzianum P1
journal, May 1999


The role of an extracellular chitinase from Trichoderma virens Gv29-8 in the biocontrol of Rhizoctonia solani
journal, February 1999

  • Baek, Jong-Min; Howell, Charles R.; Kenerley, C. M.
  • Current Genetics, Vol. 35, Issue 1
  • DOI: 10.1007/s002940050431

Works referencing / citing this record:

Insights on the Evolution of Mycoparasitism from the Genome of Clonostachys rosea
journal, January 2015

  • Karlsson, Magnus; Durling, Mikael Brandström; Choi, Jaeyoung
  • Genome Biology and Evolution, Vol. 7, Issue 2
  • DOI: 10.1093/gbe/evu292

Trichoderma: the genomics of opportunistic success
journal, September 2011

  • Druzhinina, Irina S.; Seidl-Seiboth, Verena; Herrera-Estrella, Alfredo
  • Nature Reviews Microbiology, Vol. 9, Issue 10
  • DOI: 10.1038/nrmicro2637

Comparative Genomics Provide Insights into Evolution of Trichoderma Nutrition Style
journal, January 2014

  • Xie, Bin-Bin; Qin, Qi-Long; Shi, Mei
  • Genome Biology and Evolution, Vol. 6, Issue 2
  • DOI: 10.1093/gbe/evu018

Comparative Genomics Provide Insights into Evolution of Trichoderma Nutrition Style
journal, January 2014

  • Xie, Bin-Bin; Qin, Qi-Long; Shi, Mei
  • Genome Biology and Evolution, Vol. 6, Issue 2
  • DOI: 10.1093/gbe/evu018

Bacterial and fungal chitinase chiJ orthologs evolve under different selective constraints following horizontal gene transfer
journal, October 2012


Encapsulation of Trichoderma harzianum Preserves Enzymatic Activity and Enhances the Potential for Biological Control
journal, March 2020

  • Maruyama, Cintia Rodrigues; Bilesky-José, Natália; de Lima, Renata
  • Frontiers in Bioengineering and Biotechnology, Vol. 8
  • DOI: 10.3389/fbioe.2020.00225

Insights on the Evolution of Mycoparasitism from the Genome of Clonostachys rosea
journal, January 2015

  • Karlsson, Magnus; Durling, Mikael Brandström; Choi, Jaeyoung
  • Genome Biology and Evolution, Vol. 7, Issue 2
  • DOI: 10.1093/gbe/evu292

Genome Sequence, Comparative Analysis, and Evolutionary Insights into Chitinases of Entomopathogenic Fungus Hirsutella thompsonii
journal, February 2015

  • Agrawal, Yamini; Khatri, Indu; Subramanian, Srikrishna
  • Genome Biology and Evolution, Vol. 7, Issue 3
  • DOI: 10.1093/gbe/evv037

Genome Sequence, Comparative Analysis, and Evolutionary Insights into Chitinases of Entomopathogenic Fungus Hirsutella thompsonii
journal, February 2015

  • Agrawal, Yamini; Khatri, Indu; Subramanian, Srikrishna
  • Genome Biology and Evolution, Vol. 7, Issue 3
  • DOI: 10.1093/gbe/evv037

Paleozoic diversification of terrestrial chitin-degrading bacterial lineages
journal, January 2019

  • Gruen, Danielle S.; Wolfe, Joanna M.; Fournier, Gregory P.
  • BMC Evolutionary Biology, Vol. 19, Issue 1
  • DOI: 10.1186/s12862-019-1357-8

Integrated Translatome and Proteome: Approach for Accurate Portraying of Widespread Multifunctional Aspects of Trichoderma
journal, August 2017


Identifying glycoside hydrolase family 18 genes in the mycoparasitic fungal species Clonostachys rosea
journal, July 2015

  • Karlsson, Magnus; Jensen, Dan Funck; Dubey, Mukesh
  • Microbiology, Vol. 161, Issue 7
  • DOI: 10.1099/mic.0.000096