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An ectomycorrhizal fungus alters sensitivity to jasmonate, salicylate, gibberellin, and ethylene in host roots.

Identifieur interne : 000568 ( Main/Exploration ); précédent : 000567; suivant : 000569

An ectomycorrhizal fungus alters sensitivity to jasmonate, salicylate, gibberellin, and ethylene in host roots.

Auteurs : Veronica Basso [France] ; Annegret Kohler [France] ; Shingo Miyauchi [France] ; Vasanth Singan [États-Unis] ; Frédéric Guinet [France] ; Jan Šimura ; Ond Ej Novák ; Kerrie W. Barry [États-Unis] ; Mojgan Amirebrahimi [États-Unis] ; Jonathan Block [France] ; Yohann Daguerre [France, Suède] ; Hyunsoo Na [États-Unis] ; Igor V. Grigoriev [États-Unis] ; Francis Martin [France, République populaire de Chine] ; Claire Veneault-Fourrey

Source :

RBID : pubmed:31834634

Abstract

The phytohormones jasmonate, gibberellin, salicylate, and ethylene regulate an interconnected reprogramming network integrating root development with plant responses against microbes. The establishment of mutualistic ectomycorrhizal symbiosis requires the suppression of plant defense responses against fungi as well as the modification of root architecture and cortical cell wall properties. Here, we investigated the contribution of phytohormones and their crosstalk to the ontogenesis of ectomycorrhizae (ECM) between grey poplar (Populus tremula x alba) roots and the fungus Laccaria bicolor. To obtain the hormonal blueprint of developing ECM, we quantified the concentrations of jasmonates, gibberellins, and salicylate via liquid chromatography-tandem mass spectrometry. Subsequently, we assessed root architecture, mycorrhizal morphology, and gene expression levels (RNA sequencing) in phytohormone-treated poplar lateral roots in the presence or absence of L. bicolor. Salicylic acid accumulated in mid-stage ECM. Exogenous phytohormone treatment affected the fungal colonization rate and/or frequency of Hartig net formation. Colonized lateral roots displayed diminished responsiveness to jasmonate but regulated some genes, implicated in defense and cell wall remodelling, that were specifically differentially expressed after jasmonate treatment. Responses to salicylate, gibberellin, and ethylene were enhanced in ECM. The dynamics of phytohormone accumulation and response suggest that jasmonate, gibberellin, salicylate, and ethylene signalling play multifaceted roles in poplar L. bicolor ectomycorrhizal development.

DOI: 10.1111/pce.13702
PubMed: 31834634


Affiliations:


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Le document en format XML

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<name sortKey="Amirebrahimi, Mojgan" sort="Amirebrahimi, Mojgan" uniqKey="Amirebrahimi M" first="Mojgan" last="Amirebrahimi">Mojgan Amirebrahimi</name>
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<name sortKey="Block, Jonathan" sort="Block, Jonathan" uniqKey="Block J" first="Jonathan" last="Block">Jonathan Block</name>
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<nlm:affiliation>Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Umeå, Sweden.</nlm:affiliation>
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<name sortKey="Na, Hyunsoo" sort="Na, Hyunsoo" uniqKey="Na H" first="Hyunsoo" last="Na">Hyunsoo Na</name>
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<nlm:affiliation>Joint Genome Institute (JGI), US Department of Energy, Walnut Creek, California.</nlm:affiliation>
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<region type="state">Californie</region>
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<name sortKey="Grigoriev, Igor V" sort="Grigoriev, Igor V" uniqKey="Grigoriev I" first="Igor V" last="Grigoriev">Igor V. Grigoriev</name>
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<nlm:affiliation>Joint Genome Institute (JGI), US Department of Energy, Walnut Creek, California.</nlm:affiliation>
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<region type="state">Californie</region>
</placeName>
<wicri:cityArea>Joint Genome Institute (JGI), US Department of Energy, Walnut Creek</wicri:cityArea>
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<nlm:affiliation>Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, California.</nlm:affiliation>
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<wicri:cityArea>Department of Plant and Microbial Biology, University of California Berkeley, Berkeley</wicri:cityArea>
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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>INRA, UMR Interactions Arbres/Microorganismes (IAM), Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (LabEx ARBRE), Centre INRA Grand-Est, University of Lorraine, Champenoux, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
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<nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, Beijing, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</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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<title xml:lang="en">An ectomycorrhizal fungus alters sensitivity to jasmonate, salicylate, gibberellin, and ethylene in host roots.</title>
<author>
<name sortKey="Basso, Veronica" sort="Basso, Veronica" uniqKey="Basso V" first="Veronica" last="Basso">Veronica Basso</name>
<affiliation wicri:level="3">
<nlm:affiliation>INRA, UMR Interactions Arbres/Microorganismes (IAM), Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (LabEx ARBRE), Centre INRA Grand-Est, University of Lorraine, Champenoux, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
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</affiliation>
</author>
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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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<nlm:affiliation>INRA, UMR Interactions Arbres/Microorganismes (IAM), Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (LabEx ARBRE), Centre INRA Grand-Est, University of Lorraine, Champenoux, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA, UMR Interactions Arbres/Microorganismes (IAM), Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (LabEx ARBRE), Centre INRA Grand-Est, University of Lorraine, Champenoux</wicri:regionArea>
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<name sortKey="Miyauchi, Shingo" sort="Miyauchi, Shingo" uniqKey="Miyauchi S" first="Shingo" last="Miyauchi">Shingo Miyauchi</name>
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<name sortKey="Singan, Vasanth" sort="Singan, Vasanth" uniqKey="Singan V" first="Vasanth" last="Singan">Vasanth Singan</name>
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</placeName>
<wicri:cityArea>Joint Genome Institute (JGI), US Department of Energy, Walnut Creek</wicri:cityArea>
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<name sortKey="Guinet, Frederic" sort="Guinet, Frederic" uniqKey="Guinet F" first="Frédéric" last="Guinet">Frédéric Guinet</name>
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<nlm:affiliation>INRA, UMR Interactions Arbres/Microorganismes (IAM), Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (LabEx ARBRE), Centre INRA Grand-Est, University of Lorraine, Champenoux, France.</nlm:affiliation>
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<name sortKey="Simura, Jan" sort="Simura, Jan" uniqKey="Simura J" first="Jan" last="Šimura">Jan Šimura</name>
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<nlm:affiliation>Laboratory of Growth, Palacký University, Faculty of Science & The Czech Academy of Sciences, Institute of Experimental Botany, Olomouc, The Czech Republic.</nlm:affiliation>
<wicri:noCountry code="subField">The Czech Republic</wicri:noCountry>
</affiliation>
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<name sortKey="Novak, Ond Ej" sort="Novak, Ond Ej" uniqKey="Novak O" first="Ond Ej" last="Novák">Ond Ej Novák</name>
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<nlm:affiliation>Laboratory of Growth, Palacký University, Faculty of Science & The Czech Academy of Sciences, Institute of Experimental Botany, Olomouc, The Czech Republic.</nlm:affiliation>
<wicri:noCountry code="subField">The Czech Republic</wicri:noCountry>
</affiliation>
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<author>
<name sortKey="Barry, Kerrie W" sort="Barry, Kerrie W" uniqKey="Barry K" first="Kerrie W" last="Barry">Kerrie W. Barry</name>
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<nlm:affiliation>Joint Genome Institute (JGI), US Department of Energy, Walnut Creek, California.</nlm:affiliation>
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<region type="state">Californie</region>
</placeName>
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<name sortKey="Amirebrahimi, Mojgan" sort="Amirebrahimi, Mojgan" uniqKey="Amirebrahimi M" first="Mojgan" last="Amirebrahimi">Mojgan Amirebrahimi</name>
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<nlm:affiliation>Joint Genome Institute (JGI), US Department of Energy, Walnut Creek, California.</nlm:affiliation>
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<placeName>
<region type="state">Californie</region>
</placeName>
<wicri:cityArea>Joint Genome Institute (JGI), US Department of Energy, Walnut Creek</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Block, Jonathan" sort="Block, Jonathan" uniqKey="Block J" first="Jonathan" last="Block">Jonathan Block</name>
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<nlm:affiliation>INRA, UMR Interactions Arbres/Microorganismes (IAM), Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (LabEx ARBRE), Centre INRA Grand-Est, University of Lorraine, Champenoux, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA, UMR Interactions Arbres/Microorganismes (IAM), Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (LabEx ARBRE), Centre INRA Grand-Est, University of Lorraine, Champenoux</wicri:regionArea>
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<settlement type="city">Champenoux</settlement>
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<name sortKey="Daguerre, Yohann" sort="Daguerre, Yohann" uniqKey="Daguerre Y" first="Yohann" last="Daguerre">Yohann Daguerre</name>
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<nlm:affiliation>INRA, UMR Interactions Arbres/Microorganismes (IAM), Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (LabEx ARBRE), Centre INRA Grand-Est, University of Lorraine, Champenoux, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA, UMR Interactions Arbres/Microorganismes (IAM), Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (LabEx ARBRE), Centre INRA Grand-Est, University of Lorraine, Champenoux</wicri:regionArea>
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<region type="region" nuts="2">Grand Est</region>
<region type="old region" nuts="2">Lorraine (région)</region>
<settlement type="city">Champenoux</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="1">
<nlm:affiliation>Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Umeå, Sweden.</nlm:affiliation>
<country xml:lang="fr">Suède</country>
<wicri:regionArea>Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Umeå</wicri:regionArea>
<wicri:noRegion>Umeå</wicri:noRegion>
</affiliation>
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<author>
<name sortKey="Na, Hyunsoo" sort="Na, Hyunsoo" uniqKey="Na H" first="Hyunsoo" last="Na">Hyunsoo Na</name>
<affiliation wicri:level="2">
<nlm:affiliation>Joint Genome Institute (JGI), US Department of Energy, Walnut Creek, California.</nlm:affiliation>
<country>États-Unis</country>
<placeName>
<region type="state">Californie</region>
</placeName>
<wicri:cityArea>Joint Genome Institute (JGI), US Department of Energy, Walnut Creek</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Grigoriev, Igor V" sort="Grigoriev, Igor V" uniqKey="Grigoriev I" first="Igor V" last="Grigoriev">Igor V. Grigoriev</name>
<affiliation wicri:level="2">
<nlm:affiliation>Joint Genome Institute (JGI), US Department of Energy, Walnut Creek, California.</nlm:affiliation>
<country>États-Unis</country>
<placeName>
<region type="state">Californie</region>
</placeName>
<wicri:cityArea>Joint Genome Institute (JGI), US Department of Energy, Walnut Creek</wicri:cityArea>
</affiliation>
<affiliation wicri:level="2">
<nlm:affiliation>Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, California.</nlm:affiliation>
<country>États-Unis</country>
<placeName>
<region type="state">Californie</region>
</placeName>
<wicri:cityArea>Department of Plant and Microbial Biology, University of California Berkeley, Berkeley</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Martin, Francis" sort="Martin, Francis" uniqKey="Martin F" first="Francis" last="Martin">Francis Martin</name>
<affiliation wicri:level="3">
<nlm:affiliation>INRA, UMR Interactions Arbres/Microorganismes (IAM), Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (LabEx ARBRE), Centre INRA Grand-Est, University of Lorraine, Champenoux, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA, UMR Interactions Arbres/Microorganismes (IAM), Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (LabEx ARBRE), Centre INRA Grand-Est, University of Lorraine, Champenoux</wicri:regionArea>
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<region type="region" nuts="2">Grand Est</region>
<region type="old region" nuts="2">Lorraine (région)</region>
<settlement type="city">Champenoux</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3">
<nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, Beijing, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, Beijing</wicri:regionArea>
<placeName>
<settlement type="city">Pékin</settlement>
</placeName>
</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>
</author>
</analytic>
<series>
<title level="j">Plant, cell & environment</title>
<idno type="eISSN">1365-3040</idno>
<imprint>
<date when="2020" type="published">2020</date>
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<div type="abstract" xml:lang="en">The phytohormones jasmonate, gibberellin, salicylate, and ethylene regulate an interconnected reprogramming network integrating root development with plant responses against microbes. The establishment of mutualistic ectomycorrhizal symbiosis requires the suppression of plant defense responses against fungi as well as the modification of root architecture and cortical cell wall properties. Here, we investigated the contribution of phytohormones and their crosstalk to the ontogenesis of ectomycorrhizae (ECM) between grey poplar (Populus tremula x alba) roots and the fungus Laccaria bicolor. To obtain the hormonal blueprint of developing ECM, we quantified the concentrations of jasmonates, gibberellins, and salicylate via liquid chromatography-tandem mass spectrometry. Subsequently, we assessed root architecture, mycorrhizal morphology, and gene expression levels (RNA sequencing) in phytohormone-treated poplar lateral roots in the presence or absence of L. bicolor. Salicylic acid accumulated in mid-stage ECM. Exogenous phytohormone treatment affected the fungal colonization rate and/or frequency of Hartig net formation. Colonized lateral roots displayed diminished responsiveness to jasmonate but regulated some genes, implicated in defense and cell wall remodelling, that were specifically differentially expressed after jasmonate treatment. Responses to salicylate, gibberellin, and ethylene were enhanced in ECM. The dynamics of phytohormone accumulation and response suggest that jasmonate, gibberellin, salicylate, and ethylene signalling play multifaceted roles in poplar L. bicolor ectomycorrhizal development.</div>
</front>
</TEI>
<pubmed>
<MedlineCitation Status="In-Process" Owner="NLM">
<PMID Version="1">31834634</PMID>
<DateRevised>
<Year>2020</Year>
<Month>06</Month>
<Day>17</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1365-3040</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>43</Volume>
<Issue>4</Issue>
<PubDate>
<Year>2020</Year>
<Month>04</Month>
</PubDate>
</JournalIssue>
<Title>Plant, cell & environment</Title>
<ISOAbbreviation>Plant Cell Environ</ISOAbbreviation>
</Journal>
<ArticleTitle>An ectomycorrhizal fungus alters sensitivity to jasmonate, salicylate, gibberellin, and ethylene in host roots.</ArticleTitle>
<Pagination>
<MedlinePgn>1047-1068</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1111/pce.13702</ELocationID>
<Abstract>
<AbstractText>The phytohormones jasmonate, gibberellin, salicylate, and ethylene regulate an interconnected reprogramming network integrating root development with plant responses against microbes. The establishment of mutualistic ectomycorrhizal symbiosis requires the suppression of plant defense responses against fungi as well as the modification of root architecture and cortical cell wall properties. Here, we investigated the contribution of phytohormones and their crosstalk to the ontogenesis of ectomycorrhizae (ECM) between grey poplar (Populus tremula x alba) roots and the fungus Laccaria bicolor. To obtain the hormonal blueprint of developing ECM, we quantified the concentrations of jasmonates, gibberellins, and salicylate via liquid chromatography-tandem mass spectrometry. Subsequently, we assessed root architecture, mycorrhizal morphology, and gene expression levels (RNA sequencing) in phytohormone-treated poplar lateral roots in the presence or absence of L. bicolor. Salicylic acid accumulated in mid-stage ECM. Exogenous phytohormone treatment affected the fungal colonization rate and/or frequency of Hartig net formation. Colonized lateral roots displayed diminished responsiveness to jasmonate but regulated some genes, implicated in defense and cell wall remodelling, that were specifically differentially expressed after jasmonate treatment. Responses to salicylate, gibberellin, and ethylene were enhanced in ECM. The dynamics of phytohormone accumulation and response suggest that jasmonate, gibberellin, salicylate, and ethylene signalling play multifaceted roles in poplar L. bicolor ectomycorrhizal development.</AbstractText>
<CopyrightInformation>© 2020 John Wiley & Sons Ltd.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Basso</LastName>
<ForeName>Veronica</ForeName>
<Initials>V</Initials>
<Identifier Source="ORCID">0000-0003-3273-1492</Identifier>
<AffiliationInfo>
<Affiliation>INRA, UMR Interactions Arbres/Microorganismes (IAM), Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (LabEx ARBRE), Centre INRA Grand-Est, University of Lorraine, Champenoux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kohler</LastName>
<ForeName>Annegret</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>INRA, UMR Interactions Arbres/Microorganismes (IAM), Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (LabEx ARBRE), Centre INRA Grand-Est, University of Lorraine, Champenoux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Miyauchi</LastName>
<ForeName>Shingo</ForeName>
<Initials>S</Initials>
<Identifier Source="ORCID">0000-0002-0620-5547</Identifier>
<AffiliationInfo>
<Affiliation>INRA, UMR Interactions Arbres/Microorganismes (IAM), Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (LabEx ARBRE), Centre INRA Grand-Est, University of Lorraine, Champenoux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Singan</LastName>
<ForeName>Vasanth</ForeName>
<Initials>V</Initials>
<AffiliationInfo>
<Affiliation>Joint Genome Institute (JGI), US Department of Energy, Walnut Creek, California.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Guinet</LastName>
<ForeName>Frédéric</ForeName>
<Initials>F</Initials>
<AffiliationInfo>
<Affiliation>INRA, UMR Interactions Arbres/Microorganismes (IAM), Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (LabEx ARBRE), Centre INRA Grand-Est, University of Lorraine, Champenoux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Šimura</LastName>
<ForeName>Jan</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Laboratory of Growth, Palacký University, Faculty of Science & The Czech Academy of Sciences, Institute of Experimental Botany, Olomouc, The Czech Republic.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Novák</LastName>
<ForeName>Ondřej</ForeName>
<Initials>O</Initials>
<AffiliationInfo>
<Affiliation>Laboratory of Growth, Palacký University, Faculty of Science & The Czech Academy of Sciences, Institute of Experimental Botany, Olomouc, The Czech Republic.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Barry</LastName>
<ForeName>Kerrie W</ForeName>
<Initials>KW</Initials>
<AffiliationInfo>
<Affiliation>Joint Genome Institute (JGI), US Department of Energy, Walnut Creek, California.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Amirebrahimi</LastName>
<ForeName>Mojgan</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Joint Genome Institute (JGI), US Department of Energy, Walnut Creek, California.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Block</LastName>
<ForeName>Jonathan</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>INRA, UMR Interactions Arbres/Microorganismes (IAM), Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (LabEx ARBRE), Centre INRA Grand-Est, University of Lorraine, Champenoux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Daguerre</LastName>
<ForeName>Yohann</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>INRA, UMR Interactions Arbres/Microorganismes (IAM), Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (LabEx ARBRE), Centre INRA Grand-Est, University of Lorraine, Champenoux, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Umeå, Sweden.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Na</LastName>
<ForeName>Hyunsoo</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>Joint Genome Institute (JGI), US Department of Energy, Walnut Creek, California.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Grigoriev</LastName>
<ForeName>Igor V</ForeName>
<Initials>IV</Initials>
<AffiliationInfo>
<Affiliation>Joint Genome Institute (JGI), US Department of Energy, Walnut Creek, California.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, California.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Martin</LastName>
<ForeName>Francis</ForeName>
<Initials>F</Initials>
<AffiliationInfo>
<Affiliation>INRA, UMR Interactions Arbres/Microorganismes (IAM), Laboratoire d'excellence Recherches Avancés sur la Biologie de l'Arbre et les Ecosystèmes Forestiers (LabEx ARBRE), Centre INRA Grand-Est, University of Lorraine, Champenoux, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, Beijing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Veneault-Fourrey</LastName>
<ForeName>Claire</ForeName>
<Initials>C</Initials>
<Identifier Source="ORCID">0000-0001-9778-2659</Identifier>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
<PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2020</Year>
<Month>02</Month>
<Day>05</Day>
</ArticleDate>
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<Country>United States</Country>
<MedlineTA>Plant Cell Environ</MedlineTA>
<NlmUniqueID>9309004</NlmUniqueID>
<ISSNLinking>0140-7791</ISSNLinking>
</MedlineJournalInfo>
<CitationSubset>IM</CitationSubset>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="Y">Laccaria bicolor</Keyword>
<Keyword MajorTopicYN="Y">Populus tremula x alba</Keyword>
<Keyword MajorTopicYN="Y">MiSSP</Keyword>
<Keyword MajorTopicYN="Y">cell wall remodelling</Keyword>
<Keyword MajorTopicYN="Y">crosstalk</Keyword>
<Keyword MajorTopicYN="Y">defense</Keyword>
<Keyword MajorTopicYN="Y">ectomycorrhizae</Keyword>
<Keyword MajorTopicYN="Y">jasmonate</Keyword>
<Keyword MajorTopicYN="Y">phytohormones</Keyword>
<Keyword MajorTopicYN="Y">symbiosis</Keyword>
</KeywordList>
</MedlineCitation>
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<PubMedPubDate PubStatus="received">
<Year>2019</Year>
<Month>07</Month>
<Day>24</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2019</Year>
<Month>12</Month>
<Day>04</Day>
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<Year>2019</Year>
<Month>12</Month>
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<name sortKey="Amirebrahimi, Mojgan" sort="Amirebrahimi, Mojgan" uniqKey="Amirebrahimi M" first="Mojgan" last="Amirebrahimi">Mojgan Amirebrahimi</name>
<name sortKey="Barry, Kerrie W" sort="Barry, Kerrie W" uniqKey="Barry K" first="Kerrie W" last="Barry">Kerrie W. Barry</name>
<name sortKey="Grigoriev, Igor V" sort="Grigoriev, Igor V" uniqKey="Grigoriev I" first="Igor V" last="Grigoriev">Igor V. Grigoriev</name>
<name sortKey="Grigoriev, Igor V" sort="Grigoriev, Igor V" uniqKey="Grigoriev I" first="Igor V" last="Grigoriev">Igor V. Grigoriev</name>
<name sortKey="Na, Hyunsoo" sort="Na, Hyunsoo" uniqKey="Na H" first="Hyunsoo" last="Na">Hyunsoo Na</name>
</country>
<country name="Suède">
<noRegion>
<name sortKey="Daguerre, Yohann" sort="Daguerre, Yohann" uniqKey="Daguerre Y" first="Yohann" last="Daguerre">Yohann Daguerre</name>
</noRegion>
</country>
<country name="République populaire de Chine">
<noRegion>
<name sortKey="Martin, Francis" sort="Martin, Francis" uniqKey="Martin F" first="Francis" last="Martin">Francis Martin</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>

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