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Ectopic expression of a loblolly pine class II 4-coumarate:CoA ligase alters soluble phenylpropanoid metabolism but not lignin biosynthesis in Populus.

Identifieur interne : 002271 ( Main/Exploration ); précédent : 002270; suivant : 002272

Ectopic expression of a loblolly pine class II 4-coumarate:CoA ligase alters soluble phenylpropanoid metabolism but not lignin biosynthesis in Populus.

Auteurs : Han-Yi Chen [États-Unis] ; Benjamin A. Babst [États-Unis] ; Batbayar Nyamdari [États-Unis] ; Hao Hu [États-Unis] ; Robert Sykes [États-Unis] ; Mark F. Davis [États-Unis] ; Scott A. Harding [États-Unis] ; Chung-Jui Tsai [États-Unis]

Source :

RBID : pubmed:25016610

Descripteurs français

English descriptors

Abstract

4-Coumarate:CoA ligase (4CL) catalyzes the formation of hydroxycinnamoyl-CoA esters for phenylpropanoid biosynthesis. Phylogenetically distinct Class I and Class II 4CL isoforms occur in angiosperms, and support lignin and non-lignin phenylpropanoid biosynthesis, respectively. In contrast, the few experimentally characterized gymnosperm 4CLs are associated with lignin biosynthesis and belong to the conifer-specific Class III. Here we report a new Pinus taeda isoform Pinta4CL3 that is phylogenetically more closely related to Class II angiosperm 4CLs than to Class III Pinta4CL1. Like angiosperm Class II 4CLs, Pinta4CL3 transcript levels were detected in foliar and root tissues but were absent in xylem, and recombinant Pinta4CL3 exhibited a substrate preference for 4-coumaric acid. Constitutive expression of Pinta4CL3 in transgenic Populus led to significant increases of hydroxycinnamoyl-quinate esters at the expense of hydroxycinnamoyl-glucose esters in green tissues. In particular, large increases of cinnamoyl-quinate in transgenic leaves suggested in vivo utilization of cinnamic acid by Pinta4CL3. Lignin was unaffected in transgenic Populus, consistent with Pinta4CL3 involvement in biosynthesis of non-structural phenylpropanoids. We discuss the in vivo cinnamic acid utilization activity of Pinta4CL3 and its adaptive significance in conifer defense. Together with phylogenetic inference, our data support an ancient origin of Class II 4CLs that pre-dates the angiosperm-gymnosperm split.

DOI: 10.1093/pcp/pcu098
PubMed: 25016610


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<term>Amino Acid Sequence (MeSH)</term>
<term>Base Sequence (MeSH)</term>
<term>Cloning, Molecular (MeSH)</term>
<term>Coenzyme A Ligases (genetics)</term>
<term>Coenzyme A Ligases (metabolism)</term>
<term>Coumaric Acids (metabolism)</term>
<term>Gene Expression (MeSH)</term>
<term>Gene Expression Regulation, Enzymologic (MeSH)</term>
<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Isoenzymes (MeSH)</term>
<term>Lignin (metabolism)</term>
<term>Molecular Sequence Data (MeSH)</term>
<term>Phylogeny (MeSH)</term>
<term>Pinus (enzymology)</term>
<term>Pinus (genetics)</term>
<term>Plant Leaves (chemistry)</term>
<term>Plant Leaves (enzymology)</term>
<term>Plant Leaves (genetics)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Plant Roots (chemistry)</term>
<term>Plant Roots (enzymology)</term>
<term>Plant Roots (genetics)</term>
<term>Populus (chemistry)</term>
<term>Populus (enzymology)</term>
<term>Populus (genetics)</term>
<term>Propanols (metabolism)</term>
<term>Propionates (MeSH)</term>
<term>Sequence Analysis, DNA (MeSH)</term>
<term>Xylem (chemistry)</term>
<term>Xylem (enzymology)</term>
<term>Xylem (genetics)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Acides coumariques (métabolisme)</term>
<term>Analyse de séquence d'ADN (MeSH)</term>
<term>Clonage moléculaire (MeSH)</term>
<term>Coenzyme A ligases (génétique)</term>
<term>Coenzyme A ligases (métabolisme)</term>
<term>Données de séquences moléculaires (MeSH)</term>
<term>Expression des gènes (MeSH)</term>
<term>Feuilles de plante (composition chimique)</term>
<term>Feuilles de plante (enzymologie)</term>
<term>Feuilles de plante (génétique)</term>
<term>Isoenzymes (MeSH)</term>
<term>Lignine (métabolisme)</term>
<term>Phylogenèse (MeSH)</term>
<term>Pinus (enzymologie)</term>
<term>Pinus (génétique)</term>
<term>Populus (composition chimique)</term>
<term>Populus (enzymologie)</term>
<term>Populus (génétique)</term>
<term>Propanols (métabolisme)</term>
<term>Propionates (MeSH)</term>
<term>Protéines végétales (génétique)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Racines de plante (composition chimique)</term>
<term>Racines de plante (enzymologie)</term>
<term>Racines de plante (génétique)</term>
<term>Régulation de l'expression des gènes codant pour des enzymes (MeSH)</term>
<term>Régulation de l'expression des gènes végétaux (MeSH)</term>
<term>Séquence d'acides aminés (MeSH)</term>
<term>Séquence nucléotidique (MeSH)</term>
<term>Xylème (composition chimique)</term>
<term>Xylème (enzymologie)</term>
<term>Xylème (génétique)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>Coenzyme A Ligases</term>
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Coenzyme A Ligases</term>
<term>Coumaric Acids</term>
<term>Lignin</term>
<term>Plant Proteins</term>
<term>Propanols</term>
</keywords>
<keywords scheme="MESH" qualifier="chemistry" xml:lang="en">
<term>Plant Leaves</term>
<term>Plant Roots</term>
<term>Populus</term>
<term>Xylem</term>
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<keywords scheme="MESH" qualifier="composition chimique" xml:lang="fr">
<term>Feuilles de plante</term>
<term>Populus</term>
<term>Racines de plante</term>
<term>Xylème</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr">
<term>Feuilles de plante</term>
<term>Pinus</term>
<term>Populus</term>
<term>Racines de plante</term>
<term>Xylème</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymology" xml:lang="en">
<term>Pinus</term>
<term>Plant Leaves</term>
<term>Plant Roots</term>
<term>Populus</term>
<term>Xylem</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Pinus</term>
<term>Plant Leaves</term>
<term>Plant Roots</term>
<term>Populus</term>
<term>Xylem</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Coenzyme A ligases</term>
<term>Feuilles de plante</term>
<term>Pinus</term>
<term>Populus</term>
<term>Protéines végétales</term>
<term>Racines de plante</term>
<term>Xylème</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Acides coumariques</term>
<term>Coenzyme A ligases</term>
<term>Lignine</term>
<term>Propanols</term>
<term>Protéines végétales</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Amino Acid Sequence</term>
<term>Base Sequence</term>
<term>Cloning, Molecular</term>
<term>Gene Expression</term>
<term>Gene Expression Regulation, Enzymologic</term>
<term>Gene Expression Regulation, Plant</term>
<term>Isoenzymes</term>
<term>Molecular Sequence Data</term>
<term>Phylogeny</term>
<term>Propionates</term>
<term>Sequence Analysis, DNA</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Analyse de séquence d'ADN</term>
<term>Clonage moléculaire</term>
<term>Données de séquences moléculaires</term>
<term>Expression des gènes</term>
<term>Isoenzymes</term>
<term>Phylogenèse</term>
<term>Propionates</term>
<term>Régulation de l'expression des gènes codant pour des enzymes</term>
<term>Régulation de l'expression des gènes végétaux</term>
<term>Séquence d'acides aminés</term>
<term>Séquence nucléotidique</term>
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<div type="abstract" xml:lang="en">4-Coumarate:CoA ligase (4CL) catalyzes the formation of hydroxycinnamoyl-CoA esters for phenylpropanoid biosynthesis. Phylogenetically distinct Class I and Class II 4CL isoforms occur in angiosperms, and support lignin and non-lignin phenylpropanoid biosynthesis, respectively. In contrast, the few experimentally characterized gymnosperm 4CLs are associated with lignin biosynthesis and belong to the conifer-specific Class III. Here we report a new Pinus taeda isoform Pinta4CL3 that is phylogenetically more closely related to Class II angiosperm 4CLs than to Class III Pinta4CL1. Like angiosperm Class II 4CLs, Pinta4CL3 transcript levels were detected in foliar and root tissues but were absent in xylem, and recombinant Pinta4CL3 exhibited a substrate preference for 4-coumaric acid. Constitutive expression of Pinta4CL3 in transgenic Populus led to significant increases of hydroxycinnamoyl-quinate esters at the expense of hydroxycinnamoyl-glucose esters in green tissues. In particular, large increases of cinnamoyl-quinate in transgenic leaves suggested in vivo utilization of cinnamic acid by Pinta4CL3. Lignin was unaffected in transgenic Populus, consistent with Pinta4CL3 involvement in biosynthesis of non-structural phenylpropanoids. We discuss the in vivo cinnamic acid utilization activity of Pinta4CL3 and its adaptive significance in conifer defense. Together with phylogenetic inference, our data support an ancient origin of Class II 4CLs that pre-dates the angiosperm-gymnosperm split. </div>
</front>
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<Title>Plant & cell physiology</Title>
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<ArticleTitle>Ectopic expression of a loblolly pine class II 4-coumarate:CoA ligase alters soluble phenylpropanoid metabolism but not lignin biosynthesis in Populus.</ArticleTitle>
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<ELocationID EIdType="doi" ValidYN="Y">10.1093/pcp/pcu098</ELocationID>
<Abstract>
<AbstractText>4-Coumarate:CoA ligase (4CL) catalyzes the formation of hydroxycinnamoyl-CoA esters for phenylpropanoid biosynthesis. Phylogenetically distinct Class I and Class II 4CL isoforms occur in angiosperms, and support lignin and non-lignin phenylpropanoid biosynthesis, respectively. In contrast, the few experimentally characterized gymnosperm 4CLs are associated with lignin biosynthesis and belong to the conifer-specific Class III. Here we report a new Pinus taeda isoform Pinta4CL3 that is phylogenetically more closely related to Class II angiosperm 4CLs than to Class III Pinta4CL1. Like angiosperm Class II 4CLs, Pinta4CL3 transcript levels were detected in foliar and root tissues but were absent in xylem, and recombinant Pinta4CL3 exhibited a substrate preference for 4-coumaric acid. Constitutive expression of Pinta4CL3 in transgenic Populus led to significant increases of hydroxycinnamoyl-quinate esters at the expense of hydroxycinnamoyl-glucose esters in green tissues. In particular, large increases of cinnamoyl-quinate in transgenic leaves suggested in vivo utilization of cinnamic acid by Pinta4CL3. Lignin was unaffected in transgenic Populus, consistent with Pinta4CL3 involvement in biosynthesis of non-structural phenylpropanoids. We discuss the in vivo cinnamic acid utilization activity of Pinta4CL3 and its adaptive significance in conifer defense. Together with phylogenetic inference, our data support an ancient origin of Class II 4CLs that pre-dates the angiosperm-gymnosperm split. </AbstractText>
<CopyrightInformation>© The Author 2014. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oup.com.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Chen</LastName>
<ForeName>Han-Yi</ForeName>
<Initials>HY</Initials>
<AffiliationInfo>
<Affiliation>School of Forest Resources and Environmental Sciences, Michigan Technological University, Houghton, MI 49931, USA Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Babst</LastName>
<ForeName>Benjamin A</ForeName>
<Initials>BA</Initials>
<AffiliationInfo>
<Affiliation>School of Forest Resources and Environmental Sciences, Michigan Technological University, Houghton, MI 49931, USA Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Present address: Biosciences Department, Brookhaven National Laboratory, Upton, NY 11973, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Nyamdari</LastName>
<ForeName>Batbayar</ForeName>
<Initials>B</Initials>
<AffiliationInfo>
<Affiliation>Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Department of Genetics, University of Georgia, Athens, GA 30602, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Hu</LastName>
<ForeName>Hao</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Department of Genetics, University of Georgia, Athens, GA 30602, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Sykes</LastName>
<ForeName>Robert</ForeName>
<Initials>R</Initials>
<AffiliationInfo>
<Affiliation>National Renewable Energy Laboratory, Golden, CO 80401, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Davis</LastName>
<ForeName>Mark F</ForeName>
<Initials>MF</Initials>
<AffiliationInfo>
<Affiliation>National Renewable Energy Laboratory, Golden, CO 80401, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Harding</LastName>
<ForeName>Scott A</ForeName>
<Initials>SA</Initials>
<AffiliationInfo>
<Affiliation>School of Forest Resources and Environmental Sciences, Michigan Technological University, Houghton, MI 49931, USA Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Department of Genetics, University of Georgia, Athens, GA 30602, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Tsai</LastName>
<ForeName>Chung-Jui</ForeName>
<Initials>CJ</Initials>
<AffiliationInfo>
<Affiliation>School of Forest Resources and Environmental Sciences, Michigan Technological University, Houghton, MI 49931, USA Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602, USA Department of Genetics, University of Georgia, Athens, GA 30602, USA cjtsai@uga.edu.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<DataBankList CompleteYN="Y">
<DataBank>
<DataBankName>GENBANK</DataBankName>
<AccessionNumberList>
<AccessionNumber>KF214457</AccessionNumber>
</AccessionNumberList>
</DataBank>
</DataBankList>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2014</Year>
<Month>07</Month>
<Day>12</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>Japan</Country>
<MedlineTA>Plant Cell Physiol</MedlineTA>
<NlmUniqueID>9430925</NlmUniqueID>
<ISSNLinking>0032-0781</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D003373">Coumaric Acids</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D007527">Isoenzymes</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D020005">Propanols</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D011422">Propionates</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0F897O3O4M</RegistryNumber>
<NameOfSubstance UI="C439395">1-phenylpropanol</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>9005-53-2</RegistryNumber>
<NameOfSubstance UI="D008031">Lignin</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 6.2.1.-</RegistryNumber>
<NameOfSubstance UI="D003066">Coenzyme A Ligases</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 6.2.1.12</RegistryNumber>
<NameOfSubstance UI="C019943">4-coumarate-CoA ligase</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>IBS9D1EU3J</RegistryNumber>
<NameOfSubstance UI="C495469">trans-3-(4'-hydroxyphenyl)-2-propenoic acid</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D000595" MajorTopicYN="N">Amino Acid Sequence</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D001483" MajorTopicYN="N">Base Sequence</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D003001" MajorTopicYN="N">Cloning, Molecular</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D003066" MajorTopicYN="N">Coenzyme A Ligases</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D003373" MajorTopicYN="N">Coumaric Acids</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D015870" MajorTopicYN="N">Gene Expression</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D015971" MajorTopicYN="N">Gene Expression Regulation, Enzymologic</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018506" MajorTopicYN="Y">Gene Expression Regulation, Plant</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D007527" MajorTopicYN="N">Isoenzymes</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008031" MajorTopicYN="N">Lignin</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008969" MajorTopicYN="N">Molecular Sequence Data</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010802" MajorTopicYN="N">Phylogeny</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D028223" MajorTopicYN="N">Pinus</DescriptorName>
<QualifierName UI="Q000201" MajorTopicYN="Y">enzymology</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018515" MajorTopicYN="N">Plant Leaves</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000201" MajorTopicYN="N">enzymology</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018517" MajorTopicYN="N">Plant Roots</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000201" MajorTopicYN="N">enzymology</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000201" MajorTopicYN="Y">enzymology</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D020005" MajorTopicYN="N">Propanols</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011422" MajorTopicYN="N">Propionates</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D017422" MajorTopicYN="N">Sequence Analysis, DNA</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D052584" MajorTopicYN="N">Xylem</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000201" MajorTopicYN="N">enzymology</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">Cinnamic acid</Keyword>
<Keyword MajorTopicYN="N">Defense</Keyword>
<Keyword MajorTopicYN="N">Phenylpropanoid</Keyword>
<Keyword MajorTopicYN="N">Pinus</Keyword>
<Keyword MajorTopicYN="N">Populus</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="entrez">
<Year>2014</Year>
<Month>7</Month>
<Day>14</Day>
<Hour>6</Hour>
<Minute>0</Minute>
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<PubMedPubDate PubStatus="pubmed">
<Year>2014</Year>
<Month>7</Month>
<Day>14</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2015</Year>
<Month>5</Month>
<Day>30</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">25016610</ArticleId>
<ArticleId IdType="pii">pcu098</ArticleId>
<ArticleId IdType="doi">10.1093/pcp/pcu098</ArticleId>
</ArticleIdList>
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</pubmed>
<affiliations>
<list>
<country>
<li>États-Unis</li>
</country>
<region>
<li>Colorado</li>
<li>Géorgie (États-Unis)</li>
<li>État de New York</li>
</region>
</list>
<tree>
<country name="États-Unis">
<region name="Géorgie (États-Unis)">
<name sortKey="Chen, Han Yi" sort="Chen, Han Yi" uniqKey="Chen H" first="Han-Yi" last="Chen">Han-Yi Chen</name>
</region>
<name sortKey="Babst, Benjamin A" sort="Babst, Benjamin A" uniqKey="Babst B" first="Benjamin A" last="Babst">Benjamin A. Babst</name>
<name sortKey="Davis, Mark F" sort="Davis, Mark F" uniqKey="Davis M" first="Mark F" last="Davis">Mark F. Davis</name>
<name sortKey="Harding, Scott A" sort="Harding, Scott A" uniqKey="Harding S" first="Scott A" last="Harding">Scott A. Harding</name>
<name sortKey="Hu, Hao" sort="Hu, Hao" uniqKey="Hu H" first="Hao" last="Hu">Hao Hu</name>
<name sortKey="Nyamdari, Batbayar" sort="Nyamdari, Batbayar" uniqKey="Nyamdari B" first="Batbayar" last="Nyamdari">Batbayar Nyamdari</name>
<name sortKey="Sykes, Robert" sort="Sykes, Robert" uniqKey="Sykes R" first="Robert" last="Sykes">Robert Sykes</name>
<name sortKey="Tsai, Chung Jui" sort="Tsai, Chung Jui" uniqKey="Tsai C" first="Chung-Jui" last="Tsai">Chung-Jui Tsai</name>
</country>
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