Populus trichocarpa encodes small, effector-like secreted proteins that are highly induced during mutualistic symbiosis.
Identifieur interne : 000F91 ( PubMed/Corpus ); précédent : 000F90; suivant : 000F92Populus trichocarpa encodes small, effector-like secreted proteins that are highly induced during mutualistic symbiosis.
Auteurs : Jonathan M. Plett ; Hengfu Yin ; Ritesh Mewalal ; Rongbin Hu ; Ting Li ; Priya Ranjan ; Sara Jawdy ; Henrique C. De Paoli ; George Butler ; Tessa Maureen Burch-Smith ; Hao-Bo Guo ; Chun Ju Chen ; Annegret Kohler ; Ian C. Anderson ; Jessy L. Labbé ; Francis Martin ; Gerald A. Tuskan ; Xiaohan YangSource :
- Scientific reports [ 2045-2322 ] ; 2017.
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
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<record><TEI><teiHeader><fileDesc><titleStmt><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><nlm:affiliation>INRA, UMR 1136 INRA-University of Lorraine, Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, INRA-Nancy, 54280, Champenoux, France.</nlm:affiliation></affiliation></author><author><name sortKey="Yin, Hengfu" sort="Yin, Hengfu" uniqKey="Yin H" first="Hengfu" last="Yin">Hengfu Yin</name><affiliation><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Mewalal, Ritesh" sort="Mewalal, Ritesh" uniqKey="Mewalal R" first="Ritesh" last="Mewalal">Ritesh Mewalal</name><affiliation><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Hu, Rongbin" sort="Hu, Rongbin" uniqKey="Hu R" first="Rongbin" last="Hu">Rongbin Hu</name><affiliation><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Li, Ting" sort="Li, Ting" uniqKey="Li T" first="Ting" last="Li">Ting Li</name><affiliation><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Ranjan, Priya" sort="Ranjan, Priya" uniqKey="Ranjan P" first="Priya" last="Ranjan">Priya Ranjan</name><affiliation><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Jawdy, Sara" sort="Jawdy, Sara" uniqKey="Jawdy S" first="Sara" last="Jawdy">Sara Jawdy</name><affiliation><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><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><affiliation><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Butler, George" sort="Butler, George" uniqKey="Butler G" first="George" last="Butler">George Butler</name><affiliation><nlm:affiliation>Department of Biochemistry & Cellular and Molecular Biology, University of Tennessee, Knoxville, TN, 37996, USA.</nlm:affiliation></affiliation></author><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><affiliation><nlm:affiliation>Department of Biochemistry & Cellular and Molecular Biology, University of Tennessee, Knoxville, TN, 37996, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Guo, Hao Bo" sort="Guo, Hao Bo" uniqKey="Guo H" first="Hao-Bo" last="Guo">Hao-Bo Guo</name><affiliation><nlm:affiliation>Department of Biochemistry & Cellular and Molecular Biology, University of Tennessee, Knoxville, TN, 37996, USA.</nlm:affiliation></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><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Kohler, Annegret" sort="Kohler, Annegret" uniqKey="Kohler A" first="Annegret" last="Kohler">Annegret Kohler</name><affiliation><nlm:affiliation>INRA, UMR 1136 INRA-University of Lorraine, Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, INRA-Nancy, 54280, Champenoux, France.</nlm:affiliation></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><nlm:affiliation>Hawkesbury Institute for the Environment, University of Western Sydney, Richmond, 2753, NSW, Australia.</nlm:affiliation></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><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Martin, Francis" sort="Martin, Francis" uniqKey="Martin F" first="Francis" last="Martin">Francis Martin</name><affiliation><nlm:affiliation>INRA, UMR 1136 INRA-University of Lorraine, Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, INRA-Nancy, 54280, Champenoux, France.</nlm:affiliation></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><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Yang, Xiaohan" sort="Yang, Xiaohan" uniqKey="Yang X" first="Xiaohan" last="Yang">Xiaohan Yang</name><affiliation><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA. yangx@ornl.gov.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2017">2017</date><idno type="RBID">pubmed:28336910</idno><idno type="pmid">28336910</idno><idno type="doi">10.1038/s41598-017-00400-8</idno><idno type="wicri:Area/PubMed/Corpus">000F91</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Corpus" wicri:corpus="PubMed">000F91</idno></publicationStmt><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><nlm:affiliation>INRA, UMR 1136 INRA-University of Lorraine, Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, INRA-Nancy, 54280, Champenoux, France.</nlm:affiliation></affiliation></author><author><name sortKey="Yin, Hengfu" sort="Yin, Hengfu" uniqKey="Yin H" first="Hengfu" last="Yin">Hengfu Yin</name><affiliation><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Mewalal, Ritesh" sort="Mewalal, Ritesh" uniqKey="Mewalal R" first="Ritesh" last="Mewalal">Ritesh Mewalal</name><affiliation><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Hu, Rongbin" sort="Hu, Rongbin" uniqKey="Hu R" first="Rongbin" last="Hu">Rongbin Hu</name><affiliation><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Li, Ting" sort="Li, Ting" uniqKey="Li T" first="Ting" last="Li">Ting Li</name><affiliation><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Ranjan, Priya" sort="Ranjan, Priya" uniqKey="Ranjan P" first="Priya" last="Ranjan">Priya Ranjan</name><affiliation><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Jawdy, Sara" sort="Jawdy, Sara" uniqKey="Jawdy S" first="Sara" last="Jawdy">Sara Jawdy</name><affiliation><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><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><affiliation><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Butler, George" sort="Butler, George" uniqKey="Butler G" first="George" last="Butler">George Butler</name><affiliation><nlm:affiliation>Department of Biochemistry & Cellular and Molecular Biology, University of Tennessee, Knoxville, TN, 37996, USA.</nlm:affiliation></affiliation></author><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><affiliation><nlm:affiliation>Department of Biochemistry & Cellular and Molecular Biology, University of Tennessee, Knoxville, TN, 37996, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Guo, Hao Bo" sort="Guo, Hao Bo" uniqKey="Guo H" first="Hao-Bo" last="Guo">Hao-Bo Guo</name><affiliation><nlm:affiliation>Department of Biochemistry & Cellular and Molecular Biology, University of Tennessee, Knoxville, TN, 37996, USA.</nlm:affiliation></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><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Kohler, Annegret" sort="Kohler, Annegret" uniqKey="Kohler A" first="Annegret" last="Kohler">Annegret Kohler</name><affiliation><nlm:affiliation>INRA, UMR 1136 INRA-University of Lorraine, Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, INRA-Nancy, 54280, Champenoux, France.</nlm:affiliation></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><nlm:affiliation>Hawkesbury Institute for the Environment, University of Western Sydney, Richmond, 2753, NSW, Australia.</nlm:affiliation></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><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Martin, Francis" sort="Martin, Francis" uniqKey="Martin F" first="Francis" last="Martin">Francis Martin</name><affiliation><nlm:affiliation>INRA, UMR 1136 INRA-University of Lorraine, Interactions Arbres/Microorganismes, Laboratory of Excellence ARBRE, INRA-Nancy, 54280, Champenoux, France.</nlm:affiliation></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><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Yang, Xiaohan" sort="Yang, Xiaohan" uniqKey="Yang X" first="Xiaohan" last="Yang">Xiaohan Yang</name><affiliation><nlm:affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA. yangx@ornl.gov.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Scientific reports</title><idno type="eISSN">2045-2322</idno><imprint><date when="2017" type="published">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><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="In-Data-Review" Owner="NLM"><PMID Version="1">28336910</PMID><DateCreated><Year>2017</Year><Month>03</Month><Day>24</Day></DateCreated><DateRevised><Year>2017</Year><Month>05</Month><Day>16</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>Mar</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">http://orcid.org/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">http://orcid.org/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">http://orcid.org/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">http://orcid.org/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">http://orcid.org/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">http://orcid.org/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">http://orcid.org/0000-0001-5207-4210</Identifier><AffiliationInfo><Affiliation>Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA. 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Version="1">24847068</PMID></CommentsCorrections></CommentsCorrectionsList></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></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2017</Year><Month>3</Month><Day>25</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2017</Year><Month>3</Month><Day>25</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">28336910</ArticleId><ArticleId IdType="doi">10.1038/s41598-017-00400-8</ArticleId><ArticleId IdType="pii">10.1038/s41598-017-00400-8</ArticleId><ArticleId 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