Downregulation of mitochondrial alternative oxidase affects chloroplast function, redox status and stress response in a marine diatom.
Identifieur interne : 000138 ( Main/Exploration ); précédent : 000137; suivant : 000139Downregulation of mitochondrial alternative oxidase affects chloroplast function, redox status and stress response in a marine diatom.
Auteurs : Omer Murik [France] ; Leila Tirichine [France] ; Judit Prihoda [France] ; Yann Thomas [France] ; Wagner L. Araújo [Allemagne] ; Andrew E. Allen [États-Unis] ; Alisdair R. Fernie [Allemagne] ; Chris Bowler [France]Source :
- The New phytologist [ 1469-8137 ] ; 2019.
Descripteurs français
- KwdFr :
- Antioxydants (métabolisme), Chloroplastes (métabolisme), Diatomées (enzymologie), Diatomées (physiologie), Glutathion (métabolisme), Mitochondries (enzymologie), Métabolomique (MeSH), Organismes aquatiques (enzymologie), Organismes aquatiques (physiologie), Oxidoreductases (métabolisme), Oxydoréduction (MeSH), Photosynthèse (MeSH), Protéines mitochondriales (métabolisme), Protéines végétales (métabolisme), Régulation négative (MeSH), Stress physiologique (MeSH), Transcriptome (génétique).
- MESH :
- enzymologie : Diatomées, Mitochondries, Organismes aquatiques.
- génétique : Transcriptome.
- métabolisme : Antioxydants, Chloroplastes, Glutathion, Oxidoreductases, Protéines mitochondriales, Protéines végétales.
- physiologie : Diatomées, Organismes aquatiques.
- Métabolomique, Oxydoréduction, Photosynthèse, Régulation négative, Stress physiologique.
English descriptors
- KwdEn :
- Antioxidants (metabolism), Aquatic Organisms (enzymology), Aquatic Organisms (physiology), Chloroplasts (metabolism), Diatoms (enzymology), Diatoms (physiology), Down-Regulation (MeSH), Glutathione (metabolism), Metabolomics (MeSH), Mitochondria (enzymology), Mitochondrial Proteins (metabolism), Oxidation-Reduction (MeSH), Oxidoreductases (metabolism), Photosynthesis (MeSH), Plant Proteins (metabolism), Stress, Physiological (MeSH), Transcriptome (genetics).
- MESH :
- chemical , metabolism : Antioxidants, Glutathione, Mitochondrial Proteins, Oxidoreductases, Plant Proteins.
- enzymology : Aquatic Organisms, Diatoms, Mitochondria.
- genetics : Transcriptome.
- metabolism : Chloroplasts.
- physiology : Aquatic Organisms, Diatoms.
- Down-Regulation, Metabolomics, Oxidation-Reduction, Photosynthesis, Stress, Physiological.
Abstract
Diatom dominance in contemporary aquatic environments indicates that they have developed unique and effective mechanisms to cope with the rapid and considerable fluctuations that characterize these environments. In view of their evolutionary history from a secondary endosymbiosis, inter-organellar regulation of biochemical activities may be of particular relevance. Diatom mitochondrial alternative oxidase (AOX) is believed to play a significant role in supplying chloroplasts with ATP produced in the mitochondria. Using the model diatom Phaeodactylum tricornutum we generated AOX knockdown lines, and followed sensitivity to stressors, photosynthesis and transcriptome and metabolome profiles of wild-type and knockdown lines. We show here that expression of the AOX gene is upregulated by various stresses including H2 O2 , heat, high light illumination, and iron or nitrogen limitation. AOX knockdown results in hypersensitivity to stress. Knockdown lines also show significantly reduced photosynthetic rates and their chloroplasts are more oxidized. Comparisons of transcriptome and metabolome profiles suggest a strong impact of AOX activity on gene expression, which is carried through to the level of the metabolome. Our data provide evidence for the involvement of mitochondrial AOX in processes central to the cell biology of diatoms, revealing that cross-talk between mitochondria and chloroplasts is crucial for maintaining sensitivity to changing environments.
DOI: 10.1111/nph.15479
PubMed: 30216452
Affiliations:
Links toward previous steps (curation, corpus...)
Le document en format XML
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Araújo</name><affiliation wicri:level="3"><nlm:affiliation>Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476, Potsdam-Golm, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476, Potsdam-Golm</wicri:regionArea><placeName><region type="land" nuts="2">Brandebourg</region><settlement type="city">Potsdam</settlement></placeName></affiliation></author><author><name sortKey="Allen, Andrew E" sort="Allen, Andrew E" uniqKey="Allen A" first="Andrew E" last="Allen">Andrew E. Allen</name><affiliation wicri:level="1"><nlm:affiliation>Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA, 92037, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA, 92037</wicri:regionArea><wicri:noRegion>92037</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Integrative Oceanography Division, Scripps Institution of Oceanography, UC San Diego, La Jolla, CA, 92037, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Integrative Oceanography Division, Scripps Institution of Oceanography, UC San Diego, La Jolla, CA, 92037</wicri:regionArea><wicri:noRegion>92037</wicri:noRegion></affiliation></author><author><name sortKey="Fernie, Alisdair R" sort="Fernie, Alisdair R" uniqKey="Fernie A" first="Alisdair R" last="Fernie">Alisdair R. Fernie</name><affiliation wicri:level="3"><nlm:affiliation>Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476, Potsdam-Golm, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476, Potsdam-Golm</wicri:regionArea><placeName><region type="land" nuts="2">Brandebourg</region><settlement type="city">Potsdam</settlement></placeName></affiliation></author><author><name sortKey="Bowler, Chris" sort="Bowler, Chris" uniqKey="Bowler C" first="Chris" last="Bowler">Chris Bowler</name><affiliation wicri:level="3"><nlm:affiliation>Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, Université PSL, 75005, Paris, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, Université PSL, 75005, Paris</wicri:regionArea><placeName><region type="region" nuts="2">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation></author></analytic><series><title level="j">The New phytologist</title><idno type="eISSN">1469-8137</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Antioxidants (metabolism)</term><term>Aquatic Organisms (enzymology)</term><term>Aquatic Organisms (physiology)</term><term>Chloroplasts (metabolism)</term><term>Diatoms (enzymology)</term><term>Diatoms (physiology)</term><term>Down-Regulation (MeSH)</term><term>Glutathione (metabolism)</term><term>Metabolomics (MeSH)</term><term>Mitochondria (enzymology)</term><term>Mitochondrial Proteins (metabolism)</term><term>Oxidation-Reduction (MeSH)</term><term>Oxidoreductases (metabolism)</term><term>Photosynthesis (MeSH)</term><term>Plant Proteins (metabolism)</term><term>Stress, Physiological (MeSH)</term><term>Transcriptome (genetics)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Antioxydants (métabolisme)</term><term>Chloroplastes (métabolisme)</term><term>Diatomées (enzymologie)</term><term>Diatomées (physiologie)</term><term>Glutathion (métabolisme)</term><term>Mitochondries (enzymologie)</term><term>Métabolomique (MeSH)</term><term>Organismes aquatiques (enzymologie)</term><term>Organismes aquatiques (physiologie)</term><term>Oxidoreductases (métabolisme)</term><term>Oxydoréduction (MeSH)</term><term>Photosynthèse (MeSH)</term><term>Protéines mitochondriales (métabolisme)</term><term>Protéines végétales (métabolisme)</term><term>Régulation négative (MeSH)</term><term>Stress physiologique (MeSH)</term><term>Transcriptome (génétique)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Antioxidants</term><term>Glutathione</term><term>Mitochondrial Proteins</term><term>Oxidoreductases</term><term>Plant Proteins</term></keywords><keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr"><term>Diatomées</term><term>Mitochondries</term><term>Organismes aquatiques</term></keywords><keywords scheme="MESH" qualifier="enzymology" xml:lang="en"><term>Aquatic Organisms</term><term>Diatoms</term><term>Mitochondria</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Transcriptome</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Transcriptome</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Chloroplasts</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Antioxydants</term><term>Chloroplastes</term><term>Glutathion</term><term>Oxidoreductases</term><term>Protéines mitochondriales</term><term>Protéines végétales</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Diatomées</term><term>Organismes aquatiques</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Aquatic Organisms</term><term>Diatoms</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Down-Regulation</term><term>Metabolomics</term><term>Oxidation-Reduction</term><term>Photosynthesis</term><term>Stress, Physiological</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Métabolomique</term><term>Oxydoréduction</term><term>Photosynthèse</term><term>Régulation négative</term><term>Stress physiologique</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Diatom dominance in contemporary aquatic environments indicates that they have developed unique and effective mechanisms to cope with the rapid and considerable fluctuations that characterize these environments. In view of their evolutionary history from a secondary endosymbiosis, inter-organellar regulation of biochemical activities may be of particular relevance. Diatom mitochondrial alternative oxidase (AOX) is believed to play a significant role in supplying chloroplasts with ATP produced in the mitochondria. Using the model diatom Phaeodactylum tricornutum we generated AOX knockdown lines, and followed sensitivity to stressors, photosynthesis and transcriptome and metabolome profiles of wild-type and knockdown lines. We show here that expression of the AOX gene is upregulated by various stresses including H<sub>2</sub> O<sub>2</sub> , heat, high light illumination, and iron or nitrogen limitation. AOX knockdown results in hypersensitivity to stress. Knockdown lines also show significantly reduced photosynthetic rates and their chloroplasts are more oxidized. Comparisons of transcriptome and metabolome profiles suggest a strong impact of AOX activity on gene expression, which is carried through to the level of the metabolome. Our data provide evidence for the involvement of mitochondrial AOX in processes central to the cell biology of diatoms, revealing that cross-talk between mitochondria and chloroplasts is crucial for maintaining sensitivity to changing environments.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">30216452</PMID><DateCompleted><Year>2020</Year><Month>01</Month><Day>21</Day></DateCompleted><DateRevised><Year>2020</Year><Month>09</Month><Day>30</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1469-8137</ISSN><JournalIssue CitedMedium="Internet"><Volume>221</Volume><Issue>3</Issue><PubDate><Year>2019</Year><Month>02</Month></PubDate></JournalIssue><Title>The New phytologist</Title><ISOAbbreviation>New Phytol</ISOAbbreviation></Journal><ArticleTitle>Downregulation of mitochondrial alternative oxidase affects chloroplast function, redox status and stress response in a marine diatom.</ArticleTitle><Pagination><MedlinePgn>1303-1316</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.15479</ELocationID><Abstract><AbstractText>Diatom dominance in contemporary aquatic environments indicates that they have developed unique and effective mechanisms to cope with the rapid and considerable fluctuations that characterize these environments. In view of their evolutionary history from a secondary endosymbiosis, inter-organellar regulation of biochemical activities may be of particular relevance. Diatom mitochondrial alternative oxidase (AOX) is believed to play a significant role in supplying chloroplasts with ATP produced in the mitochondria. Using the model diatom Phaeodactylum tricornutum we generated AOX knockdown lines, and followed sensitivity to stressors, photosynthesis and transcriptome and metabolome profiles of wild-type and knockdown lines. We show here that expression of the AOX gene is upregulated by various stresses including H<sub>2</sub> O<sub>2</sub> , heat, high light illumination, and iron or nitrogen limitation. AOX knockdown results in hypersensitivity to stress. Knockdown lines also show significantly reduced photosynthetic rates and their chloroplasts are more oxidized. Comparisons of transcriptome and metabolome profiles suggest a strong impact of AOX activity on gene expression, which is carried through to the level of the metabolome. Our data provide evidence for the involvement of mitochondrial AOX in processes central to the cell biology of diatoms, revealing that cross-talk between mitochondria and chloroplasts is crucial for maintaining sensitivity to changing environments.</AbstractText><CopyrightInformation>© 2018 The Authors. New Phytologist © 2018 New Phytologist Trust.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Murik</LastName><ForeName>Omer</ForeName><Initials>O</Initials><AffiliationInfo><Affiliation>Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, Université PSL, 75005, Paris, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tirichine</LastName><ForeName>Leila</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, Université PSL, 75005, Paris, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Prihoda</LastName><ForeName>Judit</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, Université PSL, 75005, Paris, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Thomas</LastName><ForeName>Yann</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, Université PSL, 75005, Paris, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Araújo</LastName><ForeName>Wagner L</ForeName><Initials>WL</Initials><AffiliationInfo><Affiliation>Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476, Potsdam-Golm, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Allen</LastName><ForeName>Andrew E</ForeName><Initials>AE</Initials><Identifier Source="ORCID">0000-0001-5911-6081</Identifier><AffiliationInfo><Affiliation>Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA, 92037, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Integrative Oceanography Division, Scripps Institution of Oceanography, UC San Diego, La Jolla, CA, 92037, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fernie</LastName><ForeName>Alisdair R</ForeName><Initials>AR</Initials><AffiliationInfo><Affiliation>Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476, Potsdam-Golm, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bowler</LastName><ForeName>Chris</ForeName><Initials>C</Initials><Identifier Source="ORCID">0000-0003-3835-6187</Identifier><AffiliationInfo><Affiliation>Institut de Biologie de l'Ecole Normale Supérieure (IBENS), Ecole normale supérieure, CNRS, INSERM, Université PSL, 75005, Paris, France.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>ANR-10-LABX-54</GrantID><Agency>French Government 'Investissements d'Avenir' programmes MEMO LIFE</Agency><Country>International</Country></Grant><Grant><GrantID>ANR-1253 11-IDEX-0001-02</GrantID><Agency>PSL* Research University</Agency><Country>International</Country></Grant><Grant><GrantID>ANR-11-BTBR-0008</GrantID><Agency>OCEANOMICS</Agency><Country>International</Country></Grant><Grant><GrantID>NSF-MCB-1024913</GrantID><Agency>National Science Foundation</Agency><Country>International</Country></Grant><Grant><GrantID>DE-SC00006719 and DE-SC0008593</GrantID><Agency>United States Department of Energy Genomics Science program</Agency><Country>International</Country></Grant><Grant><GrantID>GBMF3828</GrantID><Agency>Gordon and Betty Moore Foundation</Agency><Country>International</Country></Grant><Grant><Agency>Institut de France</Agency><Country>International</Country></Grant><Grant><Agency>Max Planck Society</Agency><Country>International</Country></Grant></GrantList><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>2018</Year><Month>11</Month><Day>22</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>New Phytol</MedlineTA><NlmUniqueID>9882884</NlmUniqueID><ISSNLinking>0028-646X</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D000975">Antioxidants</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D024101">Mitochondrial Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 1.-</RegistryNumber><NameOfSubstance UI="D010088">Oxidoreductases</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 1.-</RegistryNumber><NameOfSubstance UI="C088813">alternative oxidase</NameOfSubstance></Chemical><Chemical><RegistryNumber>GAN16C9B8O</RegistryNumber><NameOfSubstance UI="D005978">Glutathione</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000975" MajorTopicYN="N">Antioxidants</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D059001" MajorTopicYN="N">Aquatic Organisms</DescriptorName><QualifierName UI="Q000201" MajorTopicYN="Y">enzymology</QualifierName><QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D002736" MajorTopicYN="N">Chloroplasts</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D017377" MajorTopicYN="N">Diatoms</DescriptorName><QualifierName UI="Q000201" MajorTopicYN="Y">enzymology</QualifierName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D015536" MajorTopicYN="Y">Down-Regulation</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D005978" MajorTopicYN="N">Glutathione</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D055432" MajorTopicYN="N">Metabolomics</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008928" MajorTopicYN="N">Mitochondria</DescriptorName><QualifierName UI="Q000201" MajorTopicYN="Y">enzymology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D024101" MajorTopicYN="N">Mitochondrial Proteins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010084" MajorTopicYN="N">Oxidation-Reduction</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010088" MajorTopicYN="N">Oxidoreductases</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010788" MajorTopicYN="N">Photosynthesis</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D013312" MajorTopicYN="Y">Stress, Physiological</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D059467" MajorTopicYN="N">Transcriptome</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">alternative oxidase (AOX)</Keyword><Keyword MajorTopicYN="Y">diatoms</Keyword><Keyword MajorTopicYN="Y">metabolite profiling</Keyword><Keyword MajorTopicYN="Y">mitochondria</Keyword><Keyword MajorTopicYN="Y">oxidative stress</Keyword><Keyword MajorTopicYN="Y">photosynthesis</Keyword><Keyword MajorTopicYN="Y">transcriptome</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>05</Month><Day>14</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2018</Year><Month>09</Month><Day>03</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2018</Year><Month>9</Month><Day>15</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>1</Month><Day>22</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2018</Year><Month>9</Month><Day>15</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">30216452</ArticleId><ArticleId IdType="doi">10.1111/nph.15479</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Allemagne</li><li>France</li><li>États-Unis</li></country><region><li>Brandebourg</li><li>Île-de-France</li></region><settlement><li>Paris</li><li>Potsdam</li></settlement></list><tree><country name="France"><region name="Île-de-France"><name sortKey="Murik, Omer" sort="Murik, Omer" uniqKey="Murik O" first="Omer" last="Murik">Omer Murik</name></region><name sortKey="Bowler, Chris" sort="Bowler, Chris" uniqKey="Bowler C" first="Chris" last="Bowler">Chris Bowler</name><name sortKey="Prihoda, Judit" sort="Prihoda, Judit" uniqKey="Prihoda J" first="Judit" last="Prihoda">Judit Prihoda</name><name sortKey="Thomas, Yann" sort="Thomas, Yann" uniqKey="Thomas Y" first="Yann" last="Thomas">Yann Thomas</name><name sortKey="Tirichine, Leila" sort="Tirichine, Leila" uniqKey="Tirichine L" first="Leila" last="Tirichine">Leila Tirichine</name></country><country name="Allemagne"><region name="Brandebourg"><name sortKey="Araujo, Wagner L" sort="Araujo, Wagner L" uniqKey="Araujo W" first="Wagner L" last="Araújo">Wagner L. Araújo</name></region><name sortKey="Fernie, Alisdair R" sort="Fernie, Alisdair R" uniqKey="Fernie A" first="Alisdair R" last="Fernie">Alisdair R. Fernie</name></country><country name="États-Unis"><noRegion><name sortKey="Allen, Andrew E" sort="Allen, Andrew E" uniqKey="Allen A" first="Andrew E" last="Allen">Andrew E. Allen</name></noRegion><name sortKey="Allen, Andrew E" sort="Allen, Andrew E" uniqKey="Allen A" first="Andrew E" last="Allen">Andrew E. Allen</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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