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The ectomycorrhizal basidiomycete Laccaria bicolor releases a secreted β-1,4 endoglucanase that plays a key role in symbiosis development.

Identifieur interne : 000C38 ( Main/Exploration ); précédent : 000C37; suivant : 000C39

The ectomycorrhizal basidiomycete Laccaria bicolor releases a secreted β-1,4 endoglucanase that plays a key role in symbiosis development.

Auteurs : Feng Zhang [France] ; George E. Anasontzis [France] ; Aurore Labourel [France] ; Charlotte Champion [France] ; Mireille Haon [France] ; Minna Kemppainen [Argentine] ; Carine Commun [France] ; Aurélie Deveau [France] ; Alejandro Pardo [Argentine] ; Claire Veneault-Fourrey [France] ; Annegret Kohler [France] ; Marie-Noëlle Rosso [France] ; Bernard Henrissat [France, Arabie saoudite] ; Jean-Guy Berrin [France] ; Francis Martin [France]

Source :

RBID : pubmed:29624684

Descripteurs français

English descriptors

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


Affiliations:


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<name sortKey="Martin, Francis" sort="Martin, Francis" uniqKey="Martin F" first="Francis" last="Martin">Francis Martin</name>
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<country xml:lang="fr">France</country>
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<country xml:lang="fr">Argentine</country>
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<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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<country xml:lang="fr">France</country>
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<name sortKey="Kohler, Annegret" sort="Kohler, Annegret" uniqKey="Kohler A" first="Annegret" last="Kohler">Annegret Kohler</name>
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<country xml:lang="fr">France</country>
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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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<nlm:affiliation>INRA, Aix-Marseille Université, UMR 1163, Biodiversity and Biotechnology of Fungi, 13009, Marseille, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
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<name sortKey="Henrissat, Bernard" sort="Henrissat, Bernard" uniqKey="Henrissat B" first="Bernard" last="Henrissat">Bernard Henrissat</name>
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<settlement type="city">Marseille</settlement>
</placeName>
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<nlm:affiliation>Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia.</nlm:affiliation>
<country xml:lang="fr">Arabie saoudite</country>
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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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<name sortKey="Martin, Francis" sort="Martin, Francis" uniqKey="Martin F" first="Francis" last="Martin">Francis Martin</name>
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<nlm:affiliation>UMR 1136 INRA-Université de Lorraine 'Interactions Arbres/Microorganismes', Laboratoire d'Excellence ARBRE, Centre INRA-Lorraine, 54280, Champenoux, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
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<title level="j">The New phytologist</title>
<idno type="eISSN">1469-8137</idno>
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<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="KwdFr" xml:lang="fr">
<term>Cellulase (composition chimique)</term>
<term>Cellulase (isolement et purification)</term>
<term>Cellulase (métabolisme)</term>
<term>Cellulose (métabolisme)</term>
<term>Domaines protéiques (MeSH)</term>
<term>Hyphae (métabolisme)</term>
<term>Laccaria (enzymologie)</term>
<term>Laccaria (génétique)</term>
<term>Mannanes (métabolisme)</term>
<term>Mycorhizes (enzymologie)</term>
<term>Mycorhizes (génétique)</term>
<term>Pichia (métabolisme)</term>
<term>Protéines fongiques (composition chimique)</term>
<term>Protéines fongiques (isolement et purification)</term>
<term>Protéines fongiques (métabolisme)</term>
<term>Protéines recombinantes (métabolisme)</term>
<term>Régulation de l'expression des gènes fongiques (MeSH)</term>
<term>Saccharomyces cerevisiae (métabolisme)</term>
<term>Symbiose (physiologie)</term>
<term>Transcription génétique (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="composition chimique" xml:lang="fr">
<term>Cellulase</term>
<term>Protéines fongiques</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr">
<term>Laccaria</term>
<term>Mycorhizes</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="génétique" xml:lang="fr">
<term>Laccaria</term>
<term>Mycorhizes</term>
</keywords>
<keywords scheme="MESH" qualifier="isolement et purification" xml:lang="fr">
<term>Cellulase</term>
<term>Protéines fongiques</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="métabolisme" xml:lang="fr">
<term>Cellulase</term>
<term>Cellulose</term>
<term>Hyphae</term>
<term>Mannanes</term>
<term>Pichia</term>
<term>Protéines fongiques</term>
<term>Protéines recombinantes</term>
<term>Saccharomyces cerevisiae</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr">
<term>Symbiose</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>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Domaines protéiques</term>
<term>Régulation de l'expression des gènes fongiques</term>
<term>Transcription génétique</term>
</keywords>
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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>
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<Journal>
<ISSN IssnType="Electronic">1469-8137</ISSN>
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<Volume>220</Volume>
<Issue>4</Issue>
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<Year>2018</Year>
<Month>12</Month>
</PubDate>
</JournalIssue>
<Title>The New phytologist</Title>
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</Journal>
<ArticleTitle>The ectomycorrhizal basidiomycete Laccaria bicolor releases a secreted β-1,4 endoglucanase that plays a key role in symbiosis development.</ArticleTitle>
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<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>
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<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>
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<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>
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<LastName>Champion</LastName>
<ForeName>Charlotte</ForeName>
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<LastName>Haon</LastName>
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<LastName>Kemppainen</LastName>
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</AffiliationInfo>
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<LastName>Commun</LastName>
<ForeName>Carine</ForeName>
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<Affiliation>UMR 1136 INRA-Université de Lorraine 'Interactions Arbres/Microorganismes', Laboratoire d'Excellence ARBRE, Centre INRA-Lorraine, 54280, Champenoux, France.</Affiliation>
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<LastName>Deveau</LastName>
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<Author ValidYN="Y">
<LastName>Kohler</LastName>
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<Affiliation>UMR 1136 INRA-Université de Lorraine 'Interactions Arbres/Microorganismes', Laboratoire d'Excellence ARBRE, Centre INRA-Lorraine, 54280, Champenoux, France.</Affiliation>
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</Author>
<Author ValidYN="Y">
<LastName>Rosso</LastName>
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<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>
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<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>
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<Affiliation>INRA, Aix-Marseille Université, UMR 1163, Biodiversity and Biotechnology of Fungi, 13009, Marseille, France.</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y">
<LastName>Martin</LastName>
<ForeName>Francis</ForeName>
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<Affiliation>UMR 1136 INRA-Université de Lorraine 'Interactions Arbres/Microorganismes', Laboratoire d'Excellence ARBRE, Centre INRA-Lorraine, 54280, Champenoux, France.</Affiliation>
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<GrantID>No. FP7-26719</GrantID>
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<Country>International</Country>
</Grant>
<Grant>
<Agency>Consejo Nacional de Investigaciones Científicas y Técnicas</Agency>
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</Grant>
<Grant>
<Agency>Oak Ridge National Laboratory</Agency>
<Country>International</Country>
</Grant>
<Grant>
<Agency>Agencia Nacional de Promoción Científica y Tecnológica</Agency>
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</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>
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<MeshHeading>
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<MeshHeading>
<DescriptorName UI="D000072417" MajorTopicYN="N">Protein Domains</DescriptorName>
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<MeshHeading>
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<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>
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<Month>11</Month>
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<Year>2018</Year>
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<li>Lorraine (région)</li>
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<li>Université d'Aix-Marseille</li>
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<name sortKey="Kohler, Annegret" sort="Kohler, Annegret" uniqKey="Kohler A" first="Annegret" last="Kohler">Annegret Kohler</name>
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<name sortKey="Martin, Francis" sort="Martin, Francis" uniqKey="Martin F" first="Francis" last="Martin">Francis Martin</name>
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<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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<name sortKey="Pardo, Alejandro" sort="Pardo, Alejandro" uniqKey="Pardo A" first="Alejandro" last="Pardo">Alejandro Pardo</name>
</country>
<country name="Arabie saoudite">
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<name sortKey="Henrissat, Bernard" sort="Henrissat, Bernard" uniqKey="Henrissat B" first="Bernard" last="Henrissat">Bernard Henrissat</name>
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