PoplarV1, Main, Exploration, bibRecord, 001247

Populus trichocarpa encodes small, effector-like secreted proteins that are highly induced during mutualistic symbiosis.

Identifieur interne : 001247 ( Main/Exploration ); précédent : 001246; suivant : 001248

Populus trichocarpa encodes small, effector-like secreted proteins that are highly induced during mutualistic symbiosis.

Auteurs : Jonathan M. Plett [France, Australie] ; Hengfu Yin [États-Unis] ; Ritesh Mewalal [États-Unis] ; Rongbin Hu [États-Unis] ; Ting Li [États-Unis] ; Priya Ranjan [États-Unis] ; Sara Jawdy [États-Unis] ; Henrique C. De Paoli [États-Unis] ; George Butler [États-Unis] ; Tessa Maureen Burch-Smith [États-Unis] ; Hao-Bo Guo [États-Unis] ; Chun Ju Chen [États-Unis] ; Annegret Kohler [France] ; Ian C. Anderson [Australie] ; Jessy L. Labbé [États-Unis] ; Francis Martin [France] ; Gerald A. Tuskan [États-Unis] ; Xiaohan Yang [États-Unis]

Source :

Scientific reports [ 2045-2322 ] ; 2017.

RBID : pubmed:28336910

Descripteurs français

KwdFr :
- Laccaria (croissance et développement), Laccaria (physiologie), Modèles biologiques (MeSH), Noyau de la cellule (métabolisme), Populus (génétique), Populus (microbiologie), Populus (physiologie), Racines de plante (génétique), Racines de plante (microbiologie), Racines de plante (métabolisme), Symbiose (MeSH).
MESH :
- croissance et développement : Laccaria.
- génétique : Populus, Racines de plante.
- microbiologie : Populus, Racines de plante.
- métabolisme : Noyau de la cellule, Racines de plante.
- physiologie : Laccaria, Populus.
- Modèles biologiques, Symbiose.

English descriptors

KwdEn :
- Cell Nucleus (metabolism), Laccaria (growth & development), Laccaria (physiology), Models, Biological (MeSH), Plant Roots (genetics), Plant Roots (metabolism), Plant Roots (microbiology), Populus (genetics), Populus (microbiology), Populus (physiology), Symbiosis (MeSH).
MESH :
- genetics : Plant Roots, Populus.
- growth & development : Laccaria.
- metabolism : Cell Nucleus, Plant Roots.
- microbiology : Plant Roots, Populus.
- physiology : Laccaria, Populus.
- Models, Biological, Symbiosis.

Abstract

During symbiosis, organisms use a range of metabolic and protein-based signals to communicate. Of these protein signals, one class is defined as 'effectors', i.e., small secreted proteins (SSPs) that cause phenotypical and physiological changes in another organism. To date, protein-based effectors have been described in aphids, nematodes, fungi and bacteria. Using RNA sequencing of Populus trichocarpa roots in mutualistic symbiosis with the ectomycorrhizal fungus Laccaria bicolor, we sought to determine if host plants also contain genes encoding effector-like proteins. We identified 417 plant-encoded putative SSPs that were significantly regulated during this interaction, including 161 SSPs specific to P. trichocarpa and 15 SSPs exhibiting expansion in Populus and closely related lineages. We demonstrate that a subset of these SSPs can enter L. bicolor hyphae, localize to the nucleus and affect hyphal growth and morphology. We conclude that plants encode proteins that appear to function as effector proteins that may regulate symbiotic associations.

DOI: 10.1038/s41598-017-00400-8
PubMed: 28336910
PubMed Central: PMC5428498

Affiliations:

Links toward previous steps (curation, corpus...)

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Le document en format XML

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<author><name sortKey="De Paoli, Henrique C" sort="De Paoli, Henrique C" uniqKey="De Paoli H" first="Henrique C" last="De Paoli">Henrique C. De Paoli</name>
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<author><name sortKey="Burch Smith, Tessa Maureen" sort="Burch Smith, Tessa Maureen" uniqKey="Burch Smith T" first="Tessa Maureen" last="Burch-Smith">Tessa Maureen Burch-Smith</name>
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<author><name sortKey="Guo, Hao Bo" sort="Guo, Hao Bo" uniqKey="Guo H" first="Hao-Bo" last="Guo">Hao-Bo Guo</name>
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<author><name sortKey="Ju Chen, Chun" sort="Ju Chen, Chun" uniqKey="Ju Chen C" first="Chun" last="Ju Chen">Chun Ju Chen</name>
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<author><name sortKey="Anderson, Ian C" sort="Anderson, Ian C" uniqKey="Anderson I" first="Ian C" last="Anderson">Ian C. Anderson</name>
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<author><name sortKey="Labbe, Jessy L" sort="Labbe, Jessy L" uniqKey="Labbe J" first="Jessy L" last="Labbé">Jessy L. Labbé</name>
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<author><name sortKey="Martin, Francis" sort="Martin, Francis" uniqKey="Martin F" first="Francis" last="Martin">Francis Martin</name>
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<country xml:lang="fr">France</country>
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<author><name sortKey="Yang, Xiaohan" sort="Yang, Xiaohan" uniqKey="Yang X" first="Xiaohan" last="Yang">Xiaohan Yang</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en">Populus trichocarpa encodes small, effector-like secreted proteins that are highly induced during mutualistic symbiosis.</title>
<author><name sortKey="Plett, Jonathan M" sort="Plett, Jonathan M" uniqKey="Plett J" first="Jonathan M" last="Plett">Jonathan M. Plett</name>
<affiliation wicri:level="3"><nlm:affiliation>INRA, UMR 1136 INRA-University of Lorraine, Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, INRA-Nancy, 54280, Champenoux, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
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<affiliation wicri:level="1"><nlm:affiliation>Hawkesbury Institute for the Environment, University of Western Sydney, Richmond, 2753, NSW, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
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<author><name sortKey="Yin, Hengfu" sort="Yin, Hengfu" uniqKey="Yin H" first="Hengfu" last="Yin">Hengfu Yin</name>
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<country xml:lang="fr">États-Unis</country>
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</affiliation>
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<author><name sortKey="Mewalal, Ritesh" sort="Mewalal, Ritesh" uniqKey="Mewalal R" first="Ritesh" last="Mewalal">Ritesh Mewalal</name>
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<country xml:lang="fr">États-Unis</country>
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<author><name sortKey="Hu, Rongbin" sort="Hu, Rongbin" uniqKey="Hu R" first="Rongbin" last="Hu">Rongbin Hu</name>
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<country xml:lang="fr">États-Unis</country>
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<author><name sortKey="Li, Ting" sort="Li, Ting" uniqKey="Li T" first="Ting" last="Li">Ting Li</name>
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<country xml:lang="fr">États-Unis</country>
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<author><name sortKey="Ranjan, Priya" sort="Ranjan, Priya" uniqKey="Ranjan P" first="Priya" last="Ranjan">Priya Ranjan</name>
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<author><name sortKey="Jawdy, Sara" sort="Jawdy, Sara" uniqKey="Jawdy S" first="Sara" last="Jawdy">Sara Jawdy</name>
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<author><name sortKey="De Paoli, Henrique C" sort="De Paoli, Henrique C" uniqKey="De Paoli H" first="Henrique C" last="De Paoli">Henrique C. De Paoli</name>
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</affiliation>
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<author><name sortKey="Butler, George" sort="Butler, George" uniqKey="Butler G" first="George" last="Butler">George Butler</name>
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<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Biochemistry & Cellular and Molecular Biology, University of Tennessee, Knoxville, TN, 37996</wicri:regionArea>
<wicri:noRegion>37996</wicri:noRegion>
</affiliation>
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<author><name sortKey="Burch Smith, Tessa Maureen" sort="Burch Smith, Tessa Maureen" uniqKey="Burch Smith T" first="Tessa Maureen" last="Burch-Smith">Tessa Maureen Burch-Smith</name>
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<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Biochemistry & Cellular and Molecular Biology, University of Tennessee, Knoxville, TN, 37996</wicri:regionArea>
<wicri:noRegion>37996</wicri:noRegion>
</affiliation>
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<author><name sortKey="Guo, Hao Bo" sort="Guo, Hao Bo" uniqKey="Guo H" first="Hao-Bo" last="Guo">Hao-Bo Guo</name>
<affiliation wicri:level="1"><nlm:affiliation>Department of Biochemistry & Cellular and Molecular Biology, University of Tennessee, Knoxville, TN, 37996, USA.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Biochemistry & Cellular and Molecular Biology, University of Tennessee, Knoxville, TN, 37996</wicri:regionArea>
<wicri:noRegion>37996</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Ju Chen, Chun" sort="Ju Chen, Chun" uniqKey="Ju Chen C" first="Chun" last="Ju Chen">Chun Ju Chen</name>
<affiliation wicri:level="1"><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831</wicri:regionArea>
<wicri:noRegion>37831</wicri:noRegion>
</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>INRA, UMR 1136 INRA-University of Lorraine, Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, INRA-Nancy, 54280, Champenoux, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA, UMR 1136 INRA-University of Lorraine, Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, INRA-Nancy, 54280, 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="Anderson, Ian C" sort="Anderson, Ian C" uniqKey="Anderson I" first="Ian C" last="Anderson">Ian C. Anderson</name>
<affiliation wicri:level="1"><nlm:affiliation>Hawkesbury Institute for the Environment, University of Western Sydney, Richmond, 2753, NSW, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Hawkesbury Institute for the Environment, University of Western Sydney, Richmond, 2753, NSW</wicri:regionArea>
<wicri:noRegion>NSW</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Labbe, Jessy L" sort="Labbe, Jessy L" uniqKey="Labbe J" first="Jessy L" last="Labbé">Jessy L. Labbé</name>
<affiliation wicri:level="1"><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831</wicri:regionArea>
<wicri:noRegion>37831</wicri:noRegion>
</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 1136 INRA-University of Lorraine, Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, INRA-Nancy, 54280, Champenoux, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
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<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="Tuskan, Gerald A" sort="Tuskan, Gerald A" uniqKey="Tuskan G" first="Gerald A" last="Tuskan">Gerald A. Tuskan</name>
<affiliation wicri:level="1"><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831</wicri:regionArea>
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</affiliation>
</author>
<author><name sortKey="Yang, Xiaohan" sort="Yang, Xiaohan" uniqKey="Yang X" first="Xiaohan" last="Yang">Xiaohan Yang</name>
<affiliation wicri:level="1"><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA. yangx@ornl.gov.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831</wicri:regionArea>
<wicri:noRegion>37831</wicri:noRegion>
</affiliation>
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</analytic>
<series><title level="j">Scientific reports</title>
<idno type="eISSN">2045-2322</idno>
<imprint><date when="2017" type="published">2017</date>
</imprint>
</series>
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<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Cell Nucleus (metabolism)</term>
<term>Laccaria (growth & development)</term>
<term>Laccaria (physiology)</term>
<term>Models, Biological (MeSH)</term>
<term>Plant Roots (genetics)</term>
<term>Plant Roots (metabolism)</term>
<term>Plant Roots (microbiology)</term>
<term>Populus (genetics)</term>
<term>Populus (microbiology)</term>
<term>Populus (physiology)</term>
<term>Symbiosis (MeSH)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>Laccaria (croissance et développement)</term>
<term>Laccaria (physiologie)</term>
<term>Modèles biologiques (MeSH)</term>
<term>Noyau de la cellule (métabolisme)</term>
<term>Populus (génétique)</term>
<term>Populus (microbiologie)</term>
<term>Populus (physiologie)</term>
<term>Racines de plante (génétique)</term>
<term>Racines de plante (microbiologie)</term>
<term>Racines de plante (métabolisme)</term>
<term>Symbiose (MeSH)</term>
</keywords>
<keywords scheme="MESH" qualifier="croissance et développement" xml:lang="fr"><term>Laccaria</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Plant Roots</term>
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="growth & development" xml:lang="en"><term>Laccaria</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Populus</term>
<term>Racines de plante</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Cell Nucleus</term>
<term>Plant Roots</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr"><term>Populus</term>
<term>Racines de plante</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Plant Roots</term>
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Noyau de la cellule</term>
<term>Racines de plante</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Laccaria</term>
<term>Populus</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Laccaria</term>
<term>Populus</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Models, Biological</term>
<term>Symbiosis</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr"><term>Modèles biologiques</term>
<term>Symbiose</term>
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<front><div type="abstract" xml:lang="en">During symbiosis, organisms use a range of metabolic and protein-based signals to communicate. Of these protein signals, one class is defined as 'effectors', i.e., small secreted proteins (SSPs) that cause phenotypical and physiological changes in another organism. To date, protein-based effectors have been described in aphids, nematodes, fungi and bacteria. Using RNA sequencing of Populus trichocarpa roots in mutualistic symbiosis with the ectomycorrhizal fungus Laccaria bicolor, we sought to determine if host plants also contain genes encoding effector-like proteins. We identified 417 plant-encoded putative SSPs that were significantly regulated during this interaction, including 161 SSPs specific to P. trichocarpa and 15 SSPs exhibiting expansion in Populus and closely related lineages. We demonstrate that a subset of these SSPs can enter L. bicolor hyphae, localize to the nucleus and affect hyphal growth and morphology. We conclude that plants encode proteins that appear to function as effector proteins that may regulate symbiotic associations.</div>
</front>
</TEI>
<pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">28336910</PMID>
<DateCompleted><Year>2018</Year>
<Month>08</Month>
<Day>29</Day>
</DateCompleted>
<DateRevised><Year>2018</Year>
<Month>11</Month>
<Day>13</Day>
</DateRevised>
<Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2045-2322</ISSN>
<JournalIssue CitedMedium="Internet"><Volume>7</Volume>
<Issue>1</Issue>
<PubDate><Year>2017</Year>
<Month>03</Month>
<Day>23</Day>
</PubDate>
</JournalIssue>
<Title>Scientific reports</Title>
<ISOAbbreviation>Sci Rep</ISOAbbreviation>
</Journal>
<ArticleTitle>Populus trichocarpa encodes small, effector-like secreted proteins that are highly induced during mutualistic symbiosis.</ArticleTitle>
<Pagination><MedlinePgn>382</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1038/s41598-017-00400-8</ELocationID>
<Abstract><AbstractText>During symbiosis, organisms use a range of metabolic and protein-based signals to communicate. Of these protein signals, one class is defined as 'effectors', i.e., small secreted proteins (SSPs) that cause phenotypical and physiological changes in another organism. To date, protein-based effectors have been described in aphids, nematodes, fungi and bacteria. Using RNA sequencing of Populus trichocarpa roots in mutualistic symbiosis with the ectomycorrhizal fungus Laccaria bicolor, we sought to determine if host plants also contain genes encoding effector-like proteins. We identified 417 plant-encoded putative SSPs that were significantly regulated during this interaction, including 161 SSPs specific to P. trichocarpa and 15 SSPs exhibiting expansion in Populus and closely related lineages. We demonstrate that a subset of these SSPs can enter L. bicolor hyphae, localize to the nucleus and affect hyphal growth and morphology. We conclude that plants encode proteins that appear to function as effector proteins that may regulate symbiotic associations.</AbstractText>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Plett</LastName>
<ForeName>Jonathan M</ForeName>
<Initials>JM</Initials>
<AffiliationInfo><Affiliation>INRA, UMR 1136 INRA-University of Lorraine, Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, INRA-Nancy, 54280, Champenoux, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Hawkesbury Institute for the Environment, University of Western Sydney, Richmond, 2753, NSW, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Yin</LastName>
<ForeName>Hengfu</ForeName>
<Initials>H</Initials>
<Identifier Source="ORCID">0000-0002-0720-5311</Identifier>
<AffiliationInfo><Affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Mewalal</LastName>
<ForeName>Ritesh</ForeName>
<Initials>R</Initials>
<Identifier Source="ORCID">0000-0002-0153-2434</Identifier>
<AffiliationInfo><Affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Hu</LastName>
<ForeName>Rongbin</ForeName>
<Initials>R</Initials>
<Identifier Source="ORCID">0000-0001-5921-6891</Identifier>
<AffiliationInfo><Affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Li</LastName>
<ForeName>Ting</ForeName>
<Initials>T</Initials>
<AffiliationInfo><Affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Ranjan</LastName>
<ForeName>Priya</ForeName>
<Initials>P</Initials>
<AffiliationInfo><Affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Jawdy</LastName>
<ForeName>Sara</ForeName>
<Initials>S</Initials>
<AffiliationInfo><Affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>De Paoli</LastName>
<ForeName>Henrique C</ForeName>
<Initials>HC</Initials>
<Identifier Source="ORCID">0000-0001-8494-0603</Identifier>
<AffiliationInfo><Affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Butler</LastName>
<ForeName>George</ForeName>
<Initials>G</Initials>
<AffiliationInfo><Affiliation>Department of Biochemistry & Cellular and Molecular Biology, University of Tennessee, Knoxville, TN, 37996, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Burch-Smith</LastName>
<ForeName>Tessa Maureen</ForeName>
<Initials>TM</Initials>
<AffiliationInfo><Affiliation>Department of Biochemistry & Cellular and Molecular Biology, University of Tennessee, Knoxville, TN, 37996, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Guo</LastName>
<ForeName>Hao-Bo</ForeName>
<Initials>HB</Initials>
<AffiliationInfo><Affiliation>Department of Biochemistry & Cellular and Molecular Biology, University of Tennessee, Knoxville, TN, 37996, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Ju Chen</LastName>
<ForeName>Chun</ForeName>
<Initials>C</Initials>
<AffiliationInfo><Affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Kohler</LastName>
<ForeName>Annegret</ForeName>
<Initials>A</Initials>
<AffiliationInfo><Affiliation>INRA, UMR 1136 INRA-University of Lorraine, Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, INRA-Nancy, 54280, Champenoux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Anderson</LastName>
<ForeName>Ian C</ForeName>
<Initials>IC</Initials>
<AffiliationInfo><Affiliation>Hawkesbury Institute for the Environment, University of Western Sydney, Richmond, 2753, NSW, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Labbé</LastName>
<ForeName>Jessy L</ForeName>
<Initials>JL</Initials>
<Identifier Source="ORCID">0000-0003-0368-2054</Identifier>
<AffiliationInfo><Affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Martin</LastName>
<ForeName>Francis</ForeName>
<Initials>F</Initials>
<Identifier Source="ORCID">0000-0002-4737-3715</Identifier>
<AffiliationInfo><Affiliation>INRA, UMR 1136 INRA-University of Lorraine, Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, INRA-Nancy, 54280, Champenoux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Tuskan</LastName>
<ForeName>Gerald A</ForeName>
<Initials>GA</Initials>
<AffiliationInfo><Affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Yang</LastName>
<ForeName>Xiaohan</ForeName>
<Initials>X</Initials>
<Identifier Source="ORCID">0000-0001-5207-4210</Identifier>
<AffiliationInfo><Affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA. yangx@ornl.gov.</Affiliation>
</AffiliationInfo>
</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>2017</Year>
<Month>03</Month>
<Day>23</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo><Country>England</Country>
<MedlineTA>Sci Rep</MedlineTA>
<NlmUniqueID>101563288</NlmUniqueID>
<ISSNLinking>2045-2322</ISSNLinking>
</MedlineJournalInfo>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList><MeshHeading><DescriptorName UI="D002467" MajorTopicYN="N">Cell Nucleus</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D055399" MajorTopicYN="N">Laccaria</DescriptorName>
<QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D008954" MajorTopicYN="N">Models, Biological</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D018517" MajorTopicYN="N">Plant Roots</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D013559" MajorTopicYN="Y">Symbiosis</DescriptorName>
</MeshHeading>
</MeshHeadingList>
</MedlineCitation>
<PubmedData><History><PubMedPubDate PubStatus="received"><Year>2016</Year>
<Month>01</Month>
<Day>27</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted"><Year>2017</Year>
<Month>02</Month>
<Day>27</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez"><Year>2017</Year>
<Month>3</Month>
<Day>25</Day>
<Hour>6</Hour>
<Minute>0</Minute>
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<PubMedPubDate PubStatus="pubmed"><Year>2017</Year>
<Month>3</Month>
<Day>25</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline"><Year>2018</Year>
<Month>8</Month>
<Day>30</Day>
<Hour>6</Hour>
<Minute>0</Minute>
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Populus trichocarpa encodes small, effector-like secreted proteins that are highly induced during mutualistic symbiosis.

Populus trichocarpa encodes small, effector-like secreted proteins that are highly induced during mutualistic symbiosis.

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