The ectomycorrhizal basidiomycete Laccaria bicolor releases a secreted β-1,4 endoglucanase that plays a key role in symbiosis development.
Identifieur interne : 000926 ( Main/Corpus ); précédent : 000925; suivant : 000927The ectomycorrhizal basidiomycete Laccaria bicolor releases a secreted β-1,4 endoglucanase that plays a key role in symbiosis development.
Auteurs : Feng Zhang ; George E. Anasontzis ; Aurore Labourel ; Charlotte Champion ; Mireille Haon ; Minna Kemppainen ; Carine Commun ; Aurélie Deveau ; Alejandro Pardo ; Claire Veneault-Fourrey ; Annegret Kohler ; Marie-Noëlle Rosso ; Bernard Henrissat ; Jean-Guy Berrin ; Francis MartinSource :
- The New phytologist [ 1469-8137 ] ; 2018.
English descriptors
- KwdEn :
- Cellulase (chemistry), Cellulase (isolation & purification), Cellulase (metabolism), Cellulose (metabolism), Fungal Proteins (chemistry), Fungal Proteins (isolation & purification), Fungal Proteins (metabolism), Gene Expression Regulation, Fungal (MeSH), Hyphae (metabolism), Laccaria (enzymology), Laccaria (genetics), Mannans (metabolism), Mycorrhizae (enzymology), Mycorrhizae (genetics), Pichia (metabolism), Protein Domains (MeSH), Recombinant Proteins (metabolism), Saccharomyces cerevisiae (metabolism), Symbiosis (physiology), Transcription, Genetic (MeSH).
- MESH :
- chemical , chemistry : Cellulase, Fungal Proteins.
- chemical , isolation & purification : Cellulase, Fungal Proteins.
- chemical , metabolism : Cellulase, Cellulose, Fungal Proteins, Mannans, Recombinant Proteins.
- enzymology : Laccaria, Mycorrhizae.
- genetics : Laccaria, Mycorrhizae.
- metabolism : Hyphae, Pichia, Saccharomyces cerevisiae.
- physiology : Symbiosis.
- Gene Expression Regulation, Fungal, Protein Domains, Transcription, Genetic.
Abstract
In ectomycorrhiza, root ingress and colonization of the apoplast by colonizing hyphae is thought to rely mainly on the mechanical force that results from hyphal tip growth, but this could be enhanced by secretion of cell-wall-degrading enzymes, which have not yet been identified. The sole cellulose-binding module (CBM1) encoded in the genome of the ectomycorrhizal Laccaria bicolor is linked to a glycoside hydrolase family 5 (GH5) endoglucanase, LbGH5-CBM1. Here, we characterize LbGH5-CBM1 gene expression and the biochemical properties of its protein product. We also immunolocalized LbGH5-CBM1 by immunofluorescence confocal microscopy in poplar ectomycorrhiza. We show that LbGH5-CBM1 expression is substantially induced in ectomycorrhiza, and RNAi mutants with a decreased LbGH5-CBM1 expression have a lower ability to form ectomycorrhiza, suggesting a key role in symbiosis. Recombinant LbGH5-CBM1 displays its highest activity towards cellulose and galactomannans, but no activity toward L. bicolor cell walls. In situ localization of LbGH5-CBM1 in ectomycorrhiza reveals that the endoglucanase accumulates at the periphery of hyphae forming the Hartig net and the mantle. Our data suggest that the symbiosis-induced endoglucanase LbGH5-CBM1 is an enzymatic effector involved in cell wall remodeling during formation of the Hartig net and is an important determinant for successful symbiotic colonization.
DOI: 10.1111/nph.15113
PubMed: 29624684
Links to Exploration step
pubmed:29624684Le document en format XML
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<author><name sortKey="Deveau, Aurelie" sort="Deveau, Aurelie" uniqKey="Deveau A" first="Aurélie" last="Deveau">Aurélie Deveau</name>
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<author><name sortKey="Pardo, Alejandro" sort="Pardo, Alejandro" uniqKey="Pardo A" first="Alejandro" last="Pardo">Alejandro Pardo</name>
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<author><name sortKey="Veneault Fourrey, Claire" sort="Veneault Fourrey, Claire" uniqKey="Veneault Fourrey C" first="Claire" last="Veneault-Fourrey">Claire Veneault-Fourrey</name>
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<author><name sortKey="Kohler, Annegret" sort="Kohler, Annegret" uniqKey="Kohler A" first="Annegret" last="Kohler">Annegret Kohler</name>
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<author><name sortKey="Rosso, Marie Noelle" sort="Rosso, Marie Noelle" uniqKey="Rosso M" first="Marie-Noëlle" last="Rosso">Marie-Noëlle Rosso</name>
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<affiliation><nlm:affiliation>INRA, USC, 1408 AFMB, 13288, Marseille, France.</nlm:affiliation>
</affiliation>
<affiliation><nlm:affiliation>Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia.</nlm:affiliation>
</affiliation>
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<author><name sortKey="Berrin, Jean Guy" sort="Berrin, Jean Guy" uniqKey="Berrin J" first="Jean-Guy" last="Berrin">Jean-Guy Berrin</name>
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<author><name sortKey="Martin, Francis" sort="Martin, Francis" uniqKey="Martin F" first="Francis" last="Martin">Francis Martin</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en">The ectomycorrhizal basidiomycete Laccaria bicolor releases a secreted β-1,4 endoglucanase that plays a key role in symbiosis development.</title>
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<author><name sortKey="Anasontzis, George E" sort="Anasontzis, George E" uniqKey="Anasontzis G" first="George E" last="Anasontzis">George E. Anasontzis</name>
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<author><name sortKey="Deveau, Aurelie" sort="Deveau, Aurelie" uniqKey="Deveau A" first="Aurélie" last="Deveau">Aurélie Deveau</name>
<affiliation><nlm:affiliation>UMR 1136 INRA-Université de Lorraine 'Interactions Arbres/Microorganismes', Laboratoire d'Excellence ARBRE, Centre INRA-Lorraine, 54280, Champenoux, France.</nlm:affiliation>
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<author><name sortKey="Pardo, Alejandro" sort="Pardo, Alejandro" uniqKey="Pardo A" first="Alejandro" last="Pardo">Alejandro Pardo</name>
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<author><name sortKey="Veneault Fourrey, Claire" sort="Veneault Fourrey, Claire" uniqKey="Veneault Fourrey C" first="Claire" last="Veneault-Fourrey">Claire Veneault-Fourrey</name>
<affiliation><nlm:affiliation>UMR 1136 INRA-Université de Lorraine 'Interactions Arbres/Microorganismes', Laboratoire d'Excellence ARBRE, Centre INRA-Lorraine, 54280, Champenoux, France.</nlm:affiliation>
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<author><name sortKey="Kohler, Annegret" sort="Kohler, Annegret" uniqKey="Kohler A" first="Annegret" last="Kohler">Annegret Kohler</name>
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<author><name sortKey="Rosso, Marie Noelle" sort="Rosso, Marie Noelle" uniqKey="Rosso M" first="Marie-Noëlle" last="Rosso">Marie-Noëlle Rosso</name>
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</affiliation>
<affiliation><nlm:affiliation>Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia.</nlm:affiliation>
</affiliation>
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<author><name sortKey="Berrin, Jean Guy" sort="Berrin, Jean Guy" uniqKey="Berrin J" first="Jean-Guy" last="Berrin">Jean-Guy Berrin</name>
<affiliation><nlm:affiliation>INRA, Aix-Marseille Université, UMR 1163, Biodiversity and Biotechnology of Fungi, 13009, Marseille, France.</nlm:affiliation>
</affiliation>
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<author><name sortKey="Martin, Francis" sort="Martin, Francis" uniqKey="Martin F" first="Francis" last="Martin">Francis Martin</name>
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<series><title level="j">The New phytologist</title>
<idno type="eISSN">1469-8137</idno>
<imprint><date when="2018" type="published">2018</date>
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<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Cellulase (chemistry)</term>
<term>Cellulase (isolation & purification)</term>
<term>Cellulase (metabolism)</term>
<term>Cellulose (metabolism)</term>
<term>Fungal Proteins (chemistry)</term>
<term>Fungal Proteins (isolation & purification)</term>
<term>Fungal Proteins (metabolism)</term>
<term>Gene Expression Regulation, Fungal (MeSH)</term>
<term>Hyphae (metabolism)</term>
<term>Laccaria (enzymology)</term>
<term>Laccaria (genetics)</term>
<term>Mannans (metabolism)</term>
<term>Mycorrhizae (enzymology)</term>
<term>Mycorrhizae (genetics)</term>
<term>Pichia (metabolism)</term>
<term>Protein Domains (MeSH)</term>
<term>Recombinant Proteins (metabolism)</term>
<term>Saccharomyces cerevisiae (metabolism)</term>
<term>Symbiosis (physiology)</term>
<term>Transcription, Genetic (MeSH)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Cellulase</term>
<term>Fungal Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="isolation & purification" xml:lang="en"><term>Cellulase</term>
<term>Fungal Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Cellulase</term>
<term>Cellulose</term>
<term>Fungal Proteins</term>
<term>Mannans</term>
<term>Recombinant Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymology" xml:lang="en"><term>Laccaria</term>
<term>Mycorrhizae</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Laccaria</term>
<term>Mycorrhizae</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Hyphae</term>
<term>Pichia</term>
<term>Saccharomyces cerevisiae</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Symbiosis</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Gene Expression Regulation, Fungal</term>
<term>Protein Domains</term>
<term>Transcription, Genetic</term>
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<front><div type="abstract" xml:lang="en">In ectomycorrhiza, root ingress and colonization of the apoplast by colonizing hyphae is thought to rely mainly on the mechanical force that results from hyphal tip growth, but this could be enhanced by secretion of cell-wall-degrading enzymes, which have not yet been identified. The sole cellulose-binding module (CBM1) encoded in the genome of the ectomycorrhizal Laccaria bicolor is linked to a glycoside hydrolase family 5 (GH5) endoglucanase, LbGH5-CBM1. Here, we characterize LbGH5-CBM1 gene expression and the biochemical properties of its protein product. We also immunolocalized LbGH5-CBM1 by immunofluorescence confocal microscopy in poplar ectomycorrhiza. We show that LbGH5-CBM1 expression is substantially induced in ectomycorrhiza, and RNAi mutants with a decreased LbGH5-CBM1 expression have a lower ability to form ectomycorrhiza, suggesting a key role in symbiosis. Recombinant LbGH5-CBM1 displays its highest activity towards cellulose and galactomannans, but no activity toward L. bicolor cell walls. In situ localization of LbGH5-CBM1 in ectomycorrhiza reveals that the endoglucanase accumulates at the periphery of hyphae forming the Hartig net and the mantle. Our data suggest that the symbiosis-induced endoglucanase LbGH5-CBM1 is an enzymatic effector involved in cell wall remodeling during formation of the Hartig net and is an important determinant for successful symbiotic colonization.</div>
</front>
</TEI>
<pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">29624684</PMID>
<DateCompleted><Year>2019</Year>
<Month>09</Month>
<Day>25</Day>
</DateCompleted>
<DateRevised><Year>2020</Year>
<Month>09</Month>
<Day>30</Day>
</DateRevised>
<Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1469-8137</ISSN>
<JournalIssue CitedMedium="Internet"><Volume>220</Volume>
<Issue>4</Issue>
<PubDate><Year>2018</Year>
<Month>12</Month>
</PubDate>
</JournalIssue>
<Title>The New phytologist</Title>
<ISOAbbreviation>New Phytol</ISOAbbreviation>
</Journal>
<ArticleTitle>The ectomycorrhizal basidiomycete Laccaria bicolor releases a secreted β-1,4 endoglucanase that plays a key role in symbiosis development.</ArticleTitle>
<Pagination><MedlinePgn>1309-1321</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.15113</ELocationID>
<Abstract><AbstractText>In ectomycorrhiza, root ingress and colonization of the apoplast by colonizing hyphae is thought to rely mainly on the mechanical force that results from hyphal tip growth, but this could be enhanced by secretion of cell-wall-degrading enzymes, which have not yet been identified. The sole cellulose-binding module (CBM1) encoded in the genome of the ectomycorrhizal Laccaria bicolor is linked to a glycoside hydrolase family 5 (GH5) endoglucanase, LbGH5-CBM1. Here, we characterize LbGH5-CBM1 gene expression and the biochemical properties of its protein product. We also immunolocalized LbGH5-CBM1 by immunofluorescence confocal microscopy in poplar ectomycorrhiza. We show that LbGH5-CBM1 expression is substantially induced in ectomycorrhiza, and RNAi mutants with a decreased LbGH5-CBM1 expression have a lower ability to form ectomycorrhiza, suggesting a key role in symbiosis. Recombinant LbGH5-CBM1 displays its highest activity towards cellulose and galactomannans, but no activity toward L. bicolor cell walls. In situ localization of LbGH5-CBM1 in ectomycorrhiza reveals that the endoglucanase accumulates at the periphery of hyphae forming the Hartig net and the mantle. Our data suggest that the symbiosis-induced endoglucanase LbGH5-CBM1 is an enzymatic effector involved in cell wall remodeling during formation of the Hartig net and is an important determinant for successful symbiotic colonization.</AbstractText>
<CopyrightInformation>© 2018 The Authors. New Phytologist © 2018 New Phytologist Trust.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Zhang</LastName>
<ForeName>Feng</ForeName>
<Initials>F</Initials>
<AffiliationInfo><Affiliation>UMR 1136 INRA-Université de Lorraine 'Interactions Arbres/Microorganismes', Laboratoire d'Excellence ARBRE, Centre INRA-Lorraine, 54280, Champenoux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Anasontzis</LastName>
<ForeName>George E</ForeName>
<Initials>GE</Initials>
<Identifier Source="ORCID">0000-0002-2290-2801</Identifier>
<AffiliationInfo><Affiliation>INRA, Aix-Marseille Université, UMR 1163, Biodiversity and Biotechnology of Fungi, 13009, Marseille, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>CNRS, UMR 7257 & Architecture et Fonction des Macromolécules Biologiques, Aix-Marseille Université, Marseille, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Labourel</LastName>
<ForeName>Aurore</ForeName>
<Initials>A</Initials>
<AffiliationInfo><Affiliation>INRA, Aix-Marseille Université, UMR 1163, Biodiversity and Biotechnology of Fungi, 13009, Marseille, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Champion</LastName>
<ForeName>Charlotte</ForeName>
<Initials>C</Initials>
<AffiliationInfo><Affiliation>INRA, Aix-Marseille Université, UMR 1163, Biodiversity and Biotechnology of Fungi, 13009, Marseille, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Haon</LastName>
<ForeName>Mireille</ForeName>
<Initials>M</Initials>
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</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Kemppainen</LastName>
<ForeName>Minna</ForeName>
<Initials>M</Initials>
<AffiliationInfo><Affiliation>Laboratorio de Micología Molecular, Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes and CONICET, Bernal, Provincia de Buenos Aires, Argentina.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Commun</LastName>
<ForeName>Carine</ForeName>
<Initials>C</Initials>
<AffiliationInfo><Affiliation>UMR 1136 INRA-Université de Lorraine 'Interactions Arbres/Microorganismes', Laboratoire d'Excellence ARBRE, Centre INRA-Lorraine, 54280, Champenoux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Deveau</LastName>
<ForeName>Aurélie</ForeName>
<Initials>A</Initials>
<AffiliationInfo><Affiliation>UMR 1136 INRA-Université de Lorraine 'Interactions Arbres/Microorganismes', Laboratoire d'Excellence ARBRE, Centre INRA-Lorraine, 54280, Champenoux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Pardo</LastName>
<ForeName>Alejandro</ForeName>
<Initials>A</Initials>
<AffiliationInfo><Affiliation>Laboratorio de Micología Molecular, Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes and CONICET, Bernal, Provincia de Buenos Aires, Argentina.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Veneault-Fourrey</LastName>
<ForeName>Claire</ForeName>
<Initials>C</Initials>
<AffiliationInfo><Affiliation>UMR 1136 INRA-Université de Lorraine 'Interactions Arbres/Microorganismes', Laboratoire d'Excellence ARBRE, Centre INRA-Lorraine, 54280, Champenoux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Kohler</LastName>
<ForeName>Annegret</ForeName>
<Initials>A</Initials>
<Identifier Source="ORCID">0000-0002-9575-9567</Identifier>
<AffiliationInfo><Affiliation>UMR 1136 INRA-Université de Lorraine 'Interactions Arbres/Microorganismes', Laboratoire d'Excellence ARBRE, Centre INRA-Lorraine, 54280, Champenoux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Rosso</LastName>
<ForeName>Marie-Noëlle</ForeName>
<Initials>MN</Initials>
<AffiliationInfo><Affiliation>INRA, Aix-Marseille Université, UMR 1163, Biodiversity and Biotechnology of Fungi, 13009, Marseille, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Henrissat</LastName>
<ForeName>Bernard</ForeName>
<Initials>B</Initials>
<AffiliationInfo><Affiliation>CNRS, UMR 7257 & Architecture et Fonction des Macromolécules Biologiques, Aix-Marseille Université, Marseille, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>INRA, USC, 1408 AFMB, 13288, Marseille, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Berrin</LastName>
<ForeName>Jean-Guy</ForeName>
<Initials>JG</Initials>
<Identifier Source="ORCID">0000-0001-7570-3745</Identifier>
<AffiliationInfo><Affiliation>INRA, Aix-Marseille Université, UMR 1163, Biodiversity and Biotechnology of Fungi, 13009, Marseille, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Martin</LastName>
<ForeName>Francis</ForeName>
<Initials>F</Initials>
<Identifier Source="ORCID">0000-0002-4737-3715</Identifier>
<AffiliationInfo><Affiliation>UMR 1136 INRA-Université de Lorraine 'Interactions Arbres/Microorganismes', Laboratoire d'Excellence ARBRE, Centre INRA-Lorraine, 54280, Champenoux, France.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<DataBankList CompleteYN="Y"><DataBank><DataBankName>GENBANK</DataBankName>
<AccessionNumberList><AccessionNumber>NZ_ABFE00000000.1</AccessionNumber>
<AccessionNumber>XM_001879394.1</AccessionNumber>
<AccessionNumber>KIJ95778</AccessionNumber>
</AccessionNumberList>
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</DataBankList>
<GrantList CompleteYN="Y"><Grant><GrantID>No. FP7-26719</GrantID>
<Agency>EU's Seventh Framework Programme</Agency>
<Country>International</Country>
</Grant>
<Grant><Agency>Consejo Nacional de Investigaciones Científicas y Técnicas</Agency>
<Country>International</Country>
</Grant>
<Grant><Agency>Oak Ridge National Laboratory</Agency>
<Country>International</Country>
</Grant>
<Grant><Agency>Agencia Nacional de Promoción Científica y Tecnológica</Agency>
<Country>International</Country>
</Grant>
<Grant><GrantID>ANR-11-LABX 0002 01</GrantID>
<Agency>Agence Nationale de la Recherche</Agency>
<Country>International</Country>
</Grant>
<Grant><GrantID>ANR-14-CE06-0020</GrantID>
<Agency>Agence Nationale de la Recherche</Agency>
<Country>International</Country>
</Grant>
</GrantList>
<PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic"><Year>2018</Year>
<Month>04</Month>
<Day>06</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo><Country>England</Country>
<MedlineTA>New Phytol</MedlineTA>
<NlmUniqueID>9882884</NlmUniqueID>
<ISSNLinking>0028-646X</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList><Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D005656">Fungal Proteins</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D008351">Mannans</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D011994">Recombinant Proteins</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>9004-34-6</RegistryNumber>
<NameOfSubstance UI="D002482">Cellulose</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>EC 3.2.1.4</RegistryNumber>
<NameOfSubstance UI="D002480">Cellulase</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList><MeshHeading><DescriptorName UI="D002480" MajorTopicYN="N">Cellulase</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000302" MajorTopicYN="N">isolation & purification</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D002482" MajorTopicYN="N">Cellulose</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D005656" MajorTopicYN="N">Fungal Proteins</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000302" MajorTopicYN="N">isolation & purification</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D015966" MajorTopicYN="N">Gene Expression Regulation, Fungal</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D025301" MajorTopicYN="N">Hyphae</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D055399" MajorTopicYN="N">Laccaria</DescriptorName>
<QualifierName UI="Q000201" MajorTopicYN="Y">enzymology</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D008351" MajorTopicYN="N">Mannans</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName>
<QualifierName UI="Q000201" MajorTopicYN="Y">enzymology</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010843" MajorTopicYN="N">Pichia</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D000072417" MajorTopicYN="N">Protein Domains</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D011994" MajorTopicYN="N">Recombinant Proteins</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D012441" MajorTopicYN="N">Saccharomyces cerevisiae</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D013559" MajorTopicYN="N">Symbiosis</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D014158" MajorTopicYN="N">Transcription, Genetic</DescriptorName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">apoplastic effector</Keyword>
<Keyword MajorTopicYN="Y">carbohydrate-active enzymes</Keyword>
<Keyword MajorTopicYN="Y">cell-wall-modifying enzymes</Keyword>
<Keyword MajorTopicYN="Y">cellulase</Keyword>
<Keyword MajorTopicYN="Y">cellulose-binding domain</Keyword>
<Keyword MajorTopicYN="Y">endo-1,4-β-mannanase</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData><History><PubMedPubDate PubStatus="received"><Year>2017</Year>
<Month>11</Month>
<Day>10</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted"><Year>2018</Year>
<Month>02</Month>
<Day>11</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed"><Year>2018</Year>
<Month>4</Month>
<Day>7</Day>
<Hour>6</Hour>
<Minute>0</Minute>
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<PubMedPubDate PubStatus="medline"><Year>2019</Year>
<Month>9</Month>
<Day>26</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez"><Year>2018</Year>
<Month>4</Month>
<Day>7</Day>
<Hour>6</Hour>
<Minute>0</Minute>
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</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList><ArticleId IdType="pubmed">29624684</ArticleId>
<ArticleId IdType="doi">10.1111/nph.15113</ArticleId>
</ArticleIdList>
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