The small secreted effector protein MiSSP7.6 of Laccaria bicolor is required for the establishment of ectomycorrhizal symbiosis.
Identifieur interne : 000057 ( Main/Exploration ); précédent : 000056; suivant : 000058The small secreted effector protein MiSSP7.6 of Laccaria bicolor is required for the establishment of ectomycorrhizal symbiosis.
Auteurs : Heng Kang [République populaire de Chine, France] ; Xin Chen [République populaire de Chine] ; Minna Kemppainen [Argentine] ; Alejandro G. Pardo [Argentine] ; Claire Veneault-Fourrey [France] ; Annegret Kohler [France] ; Francis M. Martin [France]Source :
- Environmental microbiology [ 1462-2920 ] ; 2020.
Abstract
To establish and maintain a symbiotic relationship, the ectomycorrhizal fungus Laccaria bicolor releases mycorrhiza-induced small secreted proteins (MiSSPs) into host roots. Here, we have functionally characterized the MYCORRHIZA-iNDUCED SMALL SECRETED PROTEIN OF 7.6 kDa (MiSSP7.6) from L. bicolor by assessing its induced expression in ectomycorrhizae, silencing its expression by RNAi, and tracking in planta subcellular localization of its protein product. We also carried out yeast two-hybrid assays and bimolecular fluorescence complementation analysis to identify possible protein targets of the MiSSP7.6 effector in Populus roots. We showed that MiSSP7.6 expression is upregulated in ectomycorrhizal rootlets and associated extramatrical mycelium during the late stage of symbiosis development. RNAi mutants with a decreased MiSSP7.6 expression have a lower mycorrhization rate, suggesting a key role in the establishment of the symbiosis with plants. MiSSP7.6 is secreted, and it localizes both to the nuclei and cytoplasm in plant cells. MiSSP7.6 protein was shown to interact with two Populus Trihelix transcription factors. Furthermore, when coexpressed with one of the Trihelix transcription factors, MiSSP7.6 is localized to plant nuclei only. Our data suggest that MiSSP7.6 is a novel secreted symbiotic effector and is a potential determinant for ectomycorrhiza formation.
DOI: 10.1111/1462-2920.14959
PubMed: 32090429
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Martin</name><affiliation wicri:level="3"><nlm:affiliation>University of Lorraine, Institut National de la Recherche Agronomique, UMR Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRA-Grand Est, Champenoux, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>University of Lorraine, Institut National de la Recherche Agronomique, UMR Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRA-Grand Est, Champenoux</wicri:regionArea><placeName><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Lorraine (région)</region><settlement type="city">Champenoux</settlement></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:32090429</idno><idno type="pmid">32090429</idno><idno type="doi">10.1111/1462-2920.14959</idno><idno type="wicri:Area/Main/Corpus">000438</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000438</idno><idno type="wicri:Area/Main/Curation">000438</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000438</idno><idno type="wicri:Area/Main/Exploration">000438</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">The small secreted effector protein MiSSP7.6 of Laccaria bicolor is required for the establishment of ectomycorrhizal symbiosis.</title><author><name sortKey="Kang, Heng" sort="Kang, Heng" uniqKey="Kang H" first="Heng" last="Kang">Heng Kang</name><affiliation wicri:level="1"><nlm:affiliation>College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070</wicri:regionArea><wicri:noRegion>430070</wicri:noRegion></affiliation><affiliation wicri:level="3"><nlm:affiliation>University of Lorraine, Institut National de la Recherche Agronomique, UMR Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRA-Grand Est, Champenoux, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>University of Lorraine, Institut National de la Recherche Agronomique, UMR Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRA-Grand Est, Champenoux</wicri:regionArea><placeName><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Lorraine (région)</region><settlement type="city">Champenoux</settlement></placeName></affiliation></author><author><name sortKey="Chen, Xin" sort="Chen, Xin" uniqKey="Chen X" first="Xin" last="Chen">Xin Chen</name><affiliation wicri:level="1"><nlm:affiliation>College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070</wicri:regionArea><wicri:noRegion>430070</wicri:noRegion></affiliation></author><author><name sortKey="Kemppainen, Minna" sort="Kemppainen, Minna" uniqKey="Kemppainen M" first="Minna" last="Kemppainen">Minna Kemppainen</name><affiliation wicri:level="1"><nlm:affiliation>Laboratorio de Micología Molecular, Instituto de Microbiología Básica y Aplicada, Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Bernal, Provincia de Buenos Aires, Argentina.</nlm:affiliation><country xml:lang="fr">Argentine</country><wicri:regionArea>Laboratorio de Micología Molecular, Instituto de Microbiología Básica y Aplicada, Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Bernal, Provincia de Buenos Aires</wicri:regionArea><wicri:noRegion>Provincia de Buenos Aires</wicri:noRegion></affiliation></author><author><name sortKey="Pardo, Alejandro G" sort="Pardo, Alejandro G" uniqKey="Pardo A" first="Alejandro G" last="Pardo">Alejandro G. Pardo</name><affiliation wicri:level="1"><nlm:affiliation>Laboratorio de Micología Molecular, Instituto de Microbiología Básica y Aplicada, Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Bernal, Provincia de Buenos Aires, Argentina.</nlm:affiliation><country xml:lang="fr">Argentine</country><wicri:regionArea>Laboratorio de Micología Molecular, Instituto de Microbiología Básica y Aplicada, Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Bernal, Provincia de Buenos Aires</wicri:regionArea><wicri:noRegion>Provincia de Buenos Aires</wicri:noRegion></affiliation></author><author><name sortKey="Veneault Fourrey, Claire" sort="Veneault Fourrey, Claire" uniqKey="Veneault Fourrey C" first="Claire" last="Veneault-Fourrey">Claire Veneault-Fourrey</name><affiliation wicri:level="3"><nlm:affiliation>University of Lorraine, Institut National de la Recherche Agronomique, UMR Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRA-Grand Est, Champenoux, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>University of Lorraine, Institut National de la Recherche Agronomique, UMR Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRA-Grand Est, Champenoux</wicri:regionArea><placeName><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Lorraine (région)</region><settlement type="city">Champenoux</settlement></placeName></affiliation></author><author><name sortKey="Kohler, Annegret" sort="Kohler, Annegret" uniqKey="Kohler A" first="Annegret" last="Kohler">Annegret Kohler</name><affiliation wicri:level="3"><nlm:affiliation>University of Lorraine, Institut National de la Recherche Agronomique, UMR Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRA-Grand Est, Champenoux, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>University of Lorraine, Institut National de la Recherche Agronomique, UMR Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRA-Grand Est, Champenoux</wicri:regionArea><placeName><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Lorraine (région)</region><settlement type="city">Champenoux</settlement></placeName></affiliation></author><author><name sortKey="Martin, Francis M" sort="Martin, Francis M" uniqKey="Martin F" first="Francis M" last="Martin">Francis M. Martin</name><affiliation wicri:level="3"><nlm:affiliation>University of Lorraine, Institut National de la Recherche Agronomique, UMR Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRA-Grand Est, Champenoux, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>University of Lorraine, Institut National de la Recherche Agronomique, UMR Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRA-Grand Est, Champenoux</wicri:regionArea><placeName><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Lorraine (région)</region><settlement type="city">Champenoux</settlement></placeName></affiliation></author></analytic><series><title level="j">Environmental microbiology</title><idno type="eISSN">1462-2920</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">To establish and maintain a symbiotic relationship, the ectomycorrhizal fungus Laccaria bicolor releases mycorrhiza-induced small secreted proteins (MiSSPs) into host roots. Here, we have functionally characterized the MYCORRHIZA-iNDUCED SMALL SECRETED PROTEIN OF 7.6 kDa (MiSSP7.6) from L. bicolor by assessing its induced expression in ectomycorrhizae, silencing its expression by RNAi, and tracking in planta subcellular localization of its protein product. We also carried out yeast two-hybrid assays and bimolecular fluorescence complementation analysis to identify possible protein targets of the MiSSP7.6 effector in Populus roots. We showed that MiSSP7.6 expression is upregulated in ectomycorrhizal rootlets and associated extramatrical mycelium during the late stage of symbiosis development. RNAi mutants with a decreased MiSSP7.6 expression have a lower mycorrhization rate, suggesting a key role in the establishment of the symbiosis with plants. MiSSP7.6 is secreted, and it localizes both to the nuclei and cytoplasm in plant cells. MiSSP7.6 protein was shown to interact with two Populus Trihelix transcription factors. Furthermore, when coexpressed with one of the Trihelix transcription factors, MiSSP7.6 is localized to plant nuclei only. Our data suggest that MiSSP7.6 is a novel secreted symbiotic effector and is a potential determinant for ectomycorrhiza formation.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32090429</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>23</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1462-2920</ISSN><JournalIssue CitedMedium="Internet"><Volume>22</Volume><Issue>4</Issue><PubDate><Year>2020</Year><Month>04</Month></PubDate></JournalIssue><Title>Environmental microbiology</Title><ISOAbbreviation>Environ Microbiol</ISOAbbreviation></Journal><ArticleTitle>The small secreted effector protein MiSSP7.6 of Laccaria bicolor is required for the establishment of ectomycorrhizal symbiosis.</ArticleTitle><Pagination><MedlinePgn>1435-1446</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1111/1462-2920.14959</ELocationID><Abstract><AbstractText>To establish and maintain a symbiotic relationship, the ectomycorrhizal fungus Laccaria bicolor releases mycorrhiza-induced small secreted proteins (MiSSPs) into host roots. Here, we have functionally characterized the MYCORRHIZA-iNDUCED SMALL SECRETED PROTEIN OF 7.6 kDa (MiSSP7.6) from L. bicolor by assessing its induced expression in ectomycorrhizae, silencing its expression by RNAi, and tracking in planta subcellular localization of its protein product. We also carried out yeast two-hybrid assays and bimolecular fluorescence complementation analysis to identify possible protein targets of the MiSSP7.6 effector in Populus roots. We showed that MiSSP7.6 expression is upregulated in ectomycorrhizal rootlets and associated extramatrical mycelium during the late stage of symbiosis development. RNAi mutants with a decreased MiSSP7.6 expression have a lower mycorrhization rate, suggesting a key role in the establishment of the symbiosis with plants. MiSSP7.6 is secreted, and it localizes both to the nuclei and cytoplasm in plant cells. MiSSP7.6 protein was shown to interact with two Populus Trihelix transcription factors. Furthermore, when coexpressed with one of the Trihelix transcription factors, MiSSP7.6 is localized to plant nuclei only. Our data suggest that MiSSP7.6 is a novel secreted symbiotic effector and is a potential determinant for ectomycorrhiza formation.</AbstractText><CopyrightInformation>© 2020 Society for Applied Microbiology and John Wiley & Sons Ltd.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Kang</LastName><ForeName>Heng</ForeName><Initials>H</Initials><Identifier Source="ORCID">0000-0001-6460-2295</Identifier><AffiliationInfo><Affiliation>College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>University of Lorraine, Institut National de la Recherche Agronomique, UMR Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRA-Grand Est, Champenoux, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Xin</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kemppainen</LastName><ForeName>Minna</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Laboratorio de Micología Molecular, Instituto de Microbiología Básica y Aplicada, Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Bernal, Provincia de Buenos Aires, Argentina.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pardo</LastName><ForeName>Alejandro G</ForeName><Initials>AG</Initials><AffiliationInfo><Affiliation>Laboratorio de Micología Molecular, Instituto de Microbiología Básica y Aplicada, Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Bernal, Provincia de Buenos Aires, Argentina.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Veneault-Fourrey</LastName><ForeName>Claire</ForeName><Initials>C</Initials><Identifier Source="ORCID">0000-0001-9778-2659</Identifier><AffiliationInfo><Affiliation>University of Lorraine, Institut National de la Recherche Agronomique, UMR Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRA-Grand Est, Champenoux, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kohler</LastName><ForeName>Annegret</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>University of Lorraine, Institut National de la Recherche Agronomique, UMR Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRA-Grand Est, Champenoux, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Martin</LastName><ForeName>Francis M</ForeName><Initials>FM</Initials><AffiliationInfo><Affiliation>University of Lorraine, Institut National de la Recherche Agronomique, UMR Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, Centre INRA-Grand Est, Champenoux, France.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>2662015PY058</GrantID><Agency>Fundamental Research Funds for the Central Universities of China</Agency><Country>International</Country></Grant><Grant><GrantID>ANR-11-LABX-0002_ARBRE</GrantID><Agency>Laboratory of Excellence ARBRE</Agency><Country>International</Country></Grant><Grant><Agency>Agencia Nacional de Promoción Científica y Tecnológica</Agency><Country>International</Country></Grant><Grant><Agency>Consejo Nacional de Investigaciones Científicas y Técnicas</Agency><Country>International</Country></Grant><Grant><Agency>Universidad Nacional de Quilmes</Agency><Country>International</Country></Grant><Grant><Agency>Biological and Environmental Research</Agency><Country>International</Country></Grant><Grant><Agency>Office of Science</Agency><Country>International</Country></Grant><Grant><Agency>U.S. Department of Energy</Agency><Country>International</Country></Grant><Grant><Agency>Genomic Science Program</Agency><Country>International</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>03</Month><Day>02</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Environ Microbiol</MedlineTA><NlmUniqueID>100883692</NlmUniqueID><ISSNLinking>1462-2912</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>11</Month><Day>04</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>02</Month><Day>19</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>02</Month><Day>20</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>2</Month><Day>25</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>2</Month><Day>25</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>2</Month><Day>25</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32090429</ArticleId><ArticleId IdType="doi">10.1111/1462-2920.14959</ArticleId></ArticleIdList><ReferenceList><Title>References</Title><Reference><Citation>Almasi, E., Sahu, N., Krizsan, K., Balint, B., Kovacs, G.M., Kiss, B., et al. 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Martin</name><name sortKey="Veneault Fourrey, Claire" sort="Veneault Fourrey, Claire" uniqKey="Veneault Fourrey C" first="Claire" last="Veneault-Fourrey">Claire Veneault-Fourrey</name></country><country name="Argentine"><noRegion><name sortKey="Kemppainen, Minna" sort="Kemppainen, Minna" uniqKey="Kemppainen M" first="Minna" last="Kemppainen">Minna Kemppainen</name></noRegion><name sortKey="Pardo, Alejandro G" sort="Pardo, Alejandro G" uniqKey="Pardo A" first="Alejandro G" last="Pardo">Alejandro G. Pardo</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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