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Regulatory networks underlying mycorrhizal development delineated by genome-wide expression profiling and functional analysis of the transcription factor repertoire of the plant symbiotic fungus Laccaria bicolor.

Identifieur interne : 001214 ( Main/Exploration ); précédent : 001213; suivant : 001215

Regulatory networks underlying mycorrhizal development delineated by genome-wide expression profiling and functional analysis of the transcription factor repertoire of the plant symbiotic fungus Laccaria bicolor.

Auteurs : Y. Daguerre [France, Suède] ; E. Levati [Italie] ; J. Ruytinx [France, Belgique] ; E. Tisserant [France] ; E. Morin [France] ; A. Kohler [France] ; B. Montanini [Italie] ; S. Ottonello [Italie] ; A. Brun [France] ; C. Veneault-Fourrey [France] ; F. Martin [France]

Source :

RBID : pubmed:28923004

Descripteurs français

English descriptors

Abstract

BACKGROUND

Ectomycorrhizal (ECM) fungi develop a mutualistic symbiotic interaction with the roots of their host plants. During this process, they undergo a series of developmental transitions from the running hyphae in the rhizosphere to the coenocytic hyphae forming finger-like structures within the root apoplastic space. These transitions, which involve profound, symbiosis-associated metabolic changes, also entail a substantial transcriptome reprogramming with coordinated waves of differentially expressed genes. To date, little is known about the key transcriptional regulators driving these changes, and the aim of the present study was to delineate and functionally characterize the transcription factor (TF) repertoire of the model ECM fungus Laccaria bicolor.

RESULTS

We curated the L. bicolor gene models coding for transcription factors and assessed their expression and regulation in Poplar and Douglas fir ectomycorrhizae. We identified 285 TFs, 191 of which share a significant similarity with known transcriptional regulators. Expression profiling of the corresponding transcripts identified TF-encoding fungal genes differentially expressed in the ECM root tips of both host plants. The L. bicolor core set of differentially expressed TFs consists of 12 and 22 genes that are, respectively, upregulated and downregulated in symbiotic tissues. These TFs resemble known fungal regulators involved in the control of fungal invasive growth, fungal cell wall integrity, carbon and nitrogen metabolism, invasive stress response and fruiting-body development. However, this core set of mycorrhiza-regulated TFs seems to be characteristic of L. bicolor and our data suggest that each mycorrhizal fungus has evolved its own set of ECM development regulators. A subset of the above TFs was functionally validated with the use of a heterologous, transcription activation assay in yeast, which also allowed the identification of previously unknown, transcriptionally active yet secreted polypeptides designated as Secreted Transcriptional Activator Proteins (STAPs).

CONCLUSIONS

Transcriptional regulators required for ECM symbiosis development in L. bicolor have been uncovered and classified through genome-wide analysis. This study also identifies the STAPs as a new class of potential ECM effectors, highly expressed in mycorrhizae, which may be involved in the control of the symbiotic root transcriptome.


DOI: 10.1186/s12864-017-4114-7
PubMed: 28923004
PubMed Central: PMC5604158


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</affiliation>
<affiliation wicri:level="1">
<nlm:affiliation>Present address: Hasselt University, Centre for Environmental Sciences, Agoralaan building D, 3590, Diepenbeek, Belgium.</nlm:affiliation>
<country xml:lang="fr">Belgique</country>
<wicri:regionArea>Present address: Hasselt University, Centre for Environmental Sciences, Agoralaan building D, 3590, Diepenbeek</wicri:regionArea>
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<country xml:lang="fr">France</country>
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<country xml:lang="fr">France</country>
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</affiliation>
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<author>
<name sortKey="Morin, E" sort="Morin, E" uniqKey="Morin E" first="E" last="Morin">E. Morin</name>
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<nlm:affiliation>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, 54280, Champenoux, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
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<settlement type="city">Champenoux</settlement>
</placeName>
<orgName type="university">Université de Lorraine</orgName>
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<nlm:affiliation>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, F-54500 Vandoeuvre-lès-, Nancy, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, F-54500 Vandoeuvre-lès-, Nancy</wicri:regionArea>
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<settlement type="city">Nancy</settlement>
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<name sortKey="Kohler, A" sort="Kohler, A" uniqKey="Kohler A" first="A" last="Kohler">A. Kohler</name>
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<nlm:affiliation>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, 54280, Champenoux, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
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<settlement type="city">Champenoux</settlement>
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<nlm:affiliation>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, F-54500 Vandoeuvre-lès-, Nancy, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, F-54500 Vandoeuvre-lès-, Nancy</wicri:regionArea>
<placeName>
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<name sortKey="Montanini, B" sort="Montanini, B" uniqKey="Montanini B" first="B" last="Montanini">B. Montanini</name>
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<nlm:affiliation>Dipartimento di Scienze Chimiche, della Vita e della Sostenibilità Ambientale, Università degli Studi di Parma, Parco Area delle Scienze 23/A, 43124, Parma, Italy.</nlm:affiliation>
<country xml:lang="fr">Italie</country>
<wicri:regionArea>Dipartimento di Scienze Chimiche, della Vita e della Sostenibilità Ambientale, Università degli Studi di Parma, Parco Area delle Scienze 23/A, 43124, Parma</wicri:regionArea>
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<author>
<name sortKey="Ottonello, S" sort="Ottonello, S" uniqKey="Ottonello S" first="S" last="Ottonello">S. Ottonello</name>
<affiliation wicri:level="1">
<nlm:affiliation>Dipartimento di Scienze Chimiche, della Vita e della Sostenibilità Ambientale, Università degli Studi di Parma, Parco Area delle Scienze 23/A, 43124, Parma, Italy.</nlm:affiliation>
<country xml:lang="fr">Italie</country>
<wicri:regionArea>Dipartimento di Scienze Chimiche, della Vita e della Sostenibilità Ambientale, Università degli Studi di Parma, Parco Area delle Scienze 23/A, 43124, Parma</wicri:regionArea>
<wicri:noRegion>Parma</wicri:noRegion>
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<author>
<name sortKey="Brun, A" sort="Brun, A" uniqKey="Brun A" first="A" last="Brun">A. Brun</name>
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<nlm:affiliation>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, 54280, Champenoux, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, 54280, Champenoux</wicri:regionArea>
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<settlement type="city">Champenoux</settlement>
</placeName>
<orgName type="university">Université de Lorraine</orgName>
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<nlm:affiliation>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, F-54500 Vandoeuvre-lès-, Nancy, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, F-54500 Vandoeuvre-lès-, Nancy</wicri:regionArea>
<placeName>
<region type="region">Grand Est</region>
<region type="old region">Lorraine (région)</region>
<settlement type="city">Nancy</settlement>
</placeName>
<orgName type="university">Université de Lorraine</orgName>
</affiliation>
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<author>
<name sortKey="Veneault Fourrey, C" sort="Veneault Fourrey, C" uniqKey="Veneault Fourrey C" first="C" last="Veneault-Fourrey">C. Veneault-Fourrey</name>
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<nlm:affiliation>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, 54280, Champenoux, France. claire.fourrey@univ-lorraine.fr.</nlm:affiliation>
<country xml:lang="fr">France</country>
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<region type="old region" nuts="2">Lorraine (région)</region>
<settlement type="city">Champenoux</settlement>
</placeName>
<orgName type="university">Université de Lorraine</orgName>
</affiliation>
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<nlm:affiliation>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, F-54500 Vandoeuvre-lès-, Nancy, France. claire.fourrey@univ-lorraine.fr.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, F-54500 Vandoeuvre-lès-, Nancy</wicri:regionArea>
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<settlement type="city">Nancy</settlement>
</placeName>
<orgName type="university">Université de Lorraine</orgName>
</affiliation>
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<name sortKey="Martin, F" sort="Martin, F" uniqKey="Martin F" first="F" last="Martin">F. Martin</name>
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<nlm:affiliation>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, 54280, Champenoux, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
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<settlement type="city">Champenoux</settlement>
</placeName>
<orgName type="university">Université de Lorraine</orgName>
</affiliation>
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<nlm:affiliation>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, F-54500 Vandoeuvre-lès-, Nancy, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, F-54500 Vandoeuvre-lès-, Nancy</wicri:regionArea>
<placeName>
<region type="region">Grand Est</region>
<region type="old region">Lorraine (région)</region>
<settlement type="city">Nancy</settlement>
</placeName>
<orgName type="university">Université de Lorraine</orgName>
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<series>
<title level="j">BMC genomics</title>
<idno type="eISSN">1471-2164</idno>
<imprint>
<date when="2017" type="published">2017</date>
</imprint>
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<keywords scheme="KwdEn" xml:lang="en">
<term>Gene Expression Profiling (MeSH)</term>
<term>Gene Regulatory Networks (MeSH)</term>
<term>Genomics (MeSH)</term>
<term>Laccaria (genetics)</term>
<term>Laccaria (growth & development)</term>
<term>Mycorrhizae (genetics)</term>
<term>Mycorrhizae (growth & development)</term>
<term>Symbiosis (MeSH)</term>
<term>Transcription Factors (genetics)</term>
<term>Transcription Factors (metabolism)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Analyse de profil d'expression de gènes (MeSH)</term>
<term>Facteurs de transcription (génétique)</term>
<term>Facteurs de transcription (métabolisme)</term>
<term>Génomique (MeSH)</term>
<term>Laccaria (croissance et développement)</term>
<term>Laccaria (génétique)</term>
<term>Mycorhizes (croissance et développement)</term>
<term>Mycorhizes (génétique)</term>
<term>Réseaux de régulation génique (MeSH)</term>
<term>Symbiose (MeSH)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>Transcription Factors</term>
</keywords>
<keywords scheme="MESH" qualifier="croissance et développement" xml:lang="fr">
<term>Laccaria</term>
<term>Mycorhizes</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Laccaria</term>
<term>Mycorrhizae</term>
</keywords>
<keywords scheme="MESH" qualifier="growth & development" xml:lang="en">
<term>Laccaria</term>
<term>Mycorrhizae</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Facteurs de transcription</term>
<term>Laccaria</term>
<term>Mycorhizes</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Transcription Factors</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Facteurs de transcription</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Gene Expression Profiling</term>
<term>Gene Regulatory Networks</term>
<term>Genomics</term>
<term>Symbiosis</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Analyse de profil d'expression de gènes</term>
<term>Génomique</term>
<term>Réseaux de régulation génique</term>
<term>Symbiose</term>
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<front>
<div type="abstract" xml:lang="en">
<p>
<b>BACKGROUND</b>
</p>
<p>Ectomycorrhizal (ECM) fungi develop a mutualistic symbiotic interaction with the roots of their host plants. During this process, they undergo a series of developmental transitions from the running hyphae in the rhizosphere to the coenocytic hyphae forming finger-like structures within the root apoplastic space. These transitions, which involve profound, symbiosis-associated metabolic changes, also entail a substantial transcriptome reprogramming with coordinated waves of differentially expressed genes. To date, little is known about the key transcriptional regulators driving these changes, and the aim of the present study was to delineate and functionally characterize the transcription factor (TF) repertoire of the model ECM fungus Laccaria bicolor.</p>
</div>
<div type="abstract" xml:lang="en">
<p>
<b>RESULTS</b>
</p>
<p>We curated the L. bicolor gene models coding for transcription factors and assessed their expression and regulation in Poplar and Douglas fir ectomycorrhizae. We identified 285 TFs, 191 of which share a significant similarity with known transcriptional regulators. Expression profiling of the corresponding transcripts identified TF-encoding fungal genes differentially expressed in the ECM root tips of both host plants. The L. bicolor core set of differentially expressed TFs consists of 12 and 22 genes that are, respectively, upregulated and downregulated in symbiotic tissues. These TFs resemble known fungal regulators involved in the control of fungal invasive growth, fungal cell wall integrity, carbon and nitrogen metabolism, invasive stress response and fruiting-body development. However, this core set of mycorrhiza-regulated TFs seems to be characteristic of L. bicolor and our data suggest that each mycorrhizal fungus has evolved its own set of ECM development regulators. A subset of the above TFs was functionally validated with the use of a heterologous, transcription activation assay in yeast, which also allowed the identification of previously unknown, transcriptionally active yet secreted polypeptides designated as Secreted Transcriptional Activator Proteins (STAPs).</p>
</div>
<div type="abstract" xml:lang="en">
<p>
<b>CONCLUSIONS</b>
</p>
<p>Transcriptional regulators required for ECM symbiosis development in L. bicolor have been uncovered and classified through genome-wide analysis. This study also identifies the STAPs as a new class of potential ECM effectors, highly expressed in mycorrhizae, which may be involved in the control of the symbiotic root transcriptome.</p>
</div>
</front>
</TEI>
<pubmed>
<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">28923004</PMID>
<DateCompleted>
<Year>2018</Year>
<Month>04</Month>
<Day>30</Day>
</DateCompleted>
<DateRevised>
<Year>2018</Year>
<Month>11</Month>
<Day>13</Day>
</DateRevised>
<Article PubModel="Electronic">
<Journal>
<ISSN IssnType="Electronic">1471-2164</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>18</Volume>
<Issue>1</Issue>
<PubDate>
<Year>2017</Year>
<Month>Sep</Month>
<Day>18</Day>
</PubDate>
</JournalIssue>
<Title>BMC genomics</Title>
<ISOAbbreviation>BMC Genomics</ISOAbbreviation>
</Journal>
<ArticleTitle>Regulatory networks underlying mycorrhizal development delineated by genome-wide expression profiling and functional analysis of the transcription factor repertoire of the plant symbiotic fungus Laccaria bicolor.</ArticleTitle>
<Pagination>
<MedlinePgn>737</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1186/s12864-017-4114-7</ELocationID>
<Abstract>
<AbstractText Label="BACKGROUND" NlmCategory="BACKGROUND">Ectomycorrhizal (ECM) fungi develop a mutualistic symbiotic interaction with the roots of their host plants. During this process, they undergo a series of developmental transitions from the running hyphae in the rhizosphere to the coenocytic hyphae forming finger-like structures within the root apoplastic space. These transitions, which involve profound, symbiosis-associated metabolic changes, also entail a substantial transcriptome reprogramming with coordinated waves of differentially expressed genes. To date, little is known about the key transcriptional regulators driving these changes, and the aim of the present study was to delineate and functionally characterize the transcription factor (TF) repertoire of the model ECM fungus Laccaria bicolor.</AbstractText>
<AbstractText Label="RESULTS" NlmCategory="RESULTS">We curated the L. bicolor gene models coding for transcription factors and assessed their expression and regulation in Poplar and Douglas fir ectomycorrhizae. We identified 285 TFs, 191 of which share a significant similarity with known transcriptional regulators. Expression profiling of the corresponding transcripts identified TF-encoding fungal genes differentially expressed in the ECM root tips of both host plants. The L. bicolor core set of differentially expressed TFs consists of 12 and 22 genes that are, respectively, upregulated and downregulated in symbiotic tissues. These TFs resemble known fungal regulators involved in the control of fungal invasive growth, fungal cell wall integrity, carbon and nitrogen metabolism, invasive stress response and fruiting-body development. However, this core set of mycorrhiza-regulated TFs seems to be characteristic of L. bicolor and our data suggest that each mycorrhizal fungus has evolved its own set of ECM development regulators. A subset of the above TFs was functionally validated with the use of a heterologous, transcription activation assay in yeast, which also allowed the identification of previously unknown, transcriptionally active yet secreted polypeptides designated as Secreted Transcriptional Activator Proteins (STAPs).</AbstractText>
<AbstractText Label="CONCLUSIONS" NlmCategory="CONCLUSIONS">Transcriptional regulators required for ECM symbiosis development in L. bicolor have been uncovered and classified through genome-wide analysis. This study also identifies the STAPs as a new class of potential ECM effectors, highly expressed in mycorrhizae, which may be involved in the control of the symbiotic root transcriptome.</AbstractText>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Daguerre</LastName>
<ForeName>Y</ForeName>
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<Affiliation>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, 54280, Champenoux, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, F-54500 Vandoeuvre-lès-, Nancy, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Present address: Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, 901 83, Umea, Sweden.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Levati</LastName>
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<Initials>E</Initials>
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<Affiliation>Dipartimento di Scienze Chimiche, della Vita e della Sostenibilità Ambientale, Università degli Studi di Parma, Parco Area delle Scienze 23/A, 43124, Parma, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ruytinx</LastName>
<ForeName>J</ForeName>
<Initials>J</Initials>
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<Affiliation>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, 54280, Champenoux, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, F-54500 Vandoeuvre-lès-, Nancy, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Present address: Hasselt University, Centre for Environmental Sciences, Agoralaan building D, 3590, Diepenbeek, Belgium.</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y">
<LastName>Tisserant</LastName>
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<Affiliation>INRA, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, 54280, Champenoux, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, F-54500 Vandoeuvre-lès-, Nancy, France.</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y">
<LastName>Morin</LastName>
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</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, F-54500 Vandoeuvre-lès-, Nancy, France.</Affiliation>
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</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Université de Lorraine, UMR 1136, INRA-Université de Lorraine, Interactions Arbres/Microorganismes, Laboratoire d'Excellence ARBRE, F-54500 Vandoeuvre-lès-, Nancy, France.</Affiliation>
</AffiliationInfo>
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<LastName>Montanini</LastName>
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<Author ValidYN="Y">
<LastName>Ottonello</LastName>
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