Differential regulation of auxin and cytokinin during the secondary vascular tissue regeneration in Populus trees.
Identifieur interne : 000A27 ( Main/Exploration ); précédent : 000A26; suivant : 000A28Differential regulation of auxin and cytokinin during the secondary vascular tissue regeneration in Populus trees.
Auteurs : Jia-Jia Chen [République populaire de Chine, Finlande] ; Ling-Yan Wang [République populaire de Chine] ; Juha Immanen [Finlande] ; Kaisa Nieminen [Finlande] ; Rachel Spicer [États-Unis] ; Yk Helariutta [Finlande, Royaume-Uni] ; Jing Zhang [Finlande] ; Xin-Qiang He [République populaire de Chine]Source :
- The New phytologist [ 1469-8137 ] ; 2019.
Descripteurs français
- KwdFr :
- Acides indolacétiques (métabolisme), Arbres (génétique), Arbres (physiologie), Cambium (physiologie), Cytokinine (métabolisme), Faisceau vasculaire des plantes (physiologie), Gènes de plante (MeSH), Modèles biologiques (MeSH), Phloème (physiologie), Populus (génétique), Populus (physiologie), Régulation de l'expression des gènes végétaux (MeSH), Régénération (physiologie).
- MESH :
- génétique : Arbres, Populus.
- métabolisme : Acides indolacétiques, Cytokinine.
- physiologie : Arbres, Cambium, Faisceau vasculaire des plantes, Phloème, Populus, Régénération.
- Gènes de plante, Modèles biologiques, Régulation de l'expression des gènes végétaux.
English descriptors
- KwdEn :
- Cambium (physiology), Cytokinins (metabolism), Gene Expression Regulation, Plant (MeSH), Genes, Plant (MeSH), Indoleacetic Acids (metabolism), Models, Biological (MeSH), Phloem (physiology), Plant Vascular Bundle (physiology), Populus (genetics), Populus (physiology), Regeneration (physiology), Trees (genetics), Trees (physiology).
- MESH :
- chemical , metabolism : Cytokinins, Indoleacetic Acids.
- genetics : Populus, Trees.
- physiology : Cambium, Phloem, Plant Vascular Bundle, Populus, Regeneration, Trees.
- Gene Expression Regulation, Plant, Genes, Plant, Models, Biological.
Abstract
Tissue regeneration upon wounding in plants highlights the developmental plasticity of plants. Previous studies have described the morphological and molecular changes of secondary vascular tissue (SVT) regeneration after large-scale bark girdling in trees. However, how phytohormones regulate SVT regeneration is still unknown. Here, we established a novel in vitro SVT regeneration system in the hybrid aspen (Populus tremula × Populus tremuloides) clone T89 to bypass the limitation of using field-grown trees. The effects of phytohormones on SVT regeneration were investigated by applying exogenous hormones and utilizing various transgenic trees. Vascular tissue-specific markers and hormonal response factors were also examined during SVT regeneration. Using this in vitro regeneration system, we demonstrated that auxin and cytokinin differentially regulate phloem and cambium regeneration. Whereas auxin is sufficient to induce regeneration of phloem prior to continuous cambium restoration, cytokinin only promotes the formation of new phloem, not cambium. The positive role of cytokinin on phloem regeneration was further confirmed in cytokinin overexpression trees. Analysis of a DR5 reporter transgenic line further suggested that cytokinin blocks the re-establishment of auxin gradients, which is required for the cambium formation. Investigation on the auxin and cytokinin signalling genes indicated these two hormones interact to regulate SVT regeneration. Taken together, the in vitro SVT regeneration system allows us to make use of various molecular and genetic tools to investigate SVT regeneration. Our results confirmed that complementary auxin and cytokinin domains are required for phloem and cambium reconstruction.
DOI: 10.1111/nph.16019
PubMed: 31230359
Affiliations:
- Finlande, Royaume-Uni, République populaire de Chine, États-Unis
- Angleterre, Angleterre de l'Est, Pékin, Uusimaa
- Cambridge, Helsinki, Pékin
- Université d'Helsinki, Université de Cambridge, Université de Pékin
Links toward previous steps (curation, corpus...)
Le document en format XML
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Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing, 100871, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing, 100871</wicri:regionArea><orgName type="university">Université de Pékin</orgName><placeName><settlement type="city">Pékin</settlement><region type="capitale">Pékin</region></placeName></affiliation><affiliation wicri:level="4"><nlm:affiliation>Institute of Biotechnology, HiLIFE, University of Helsinki, Helsinki, 00014, Finland.</nlm:affiliation><country xml:lang="fr">Finlande</country><wicri:regionArea>Institute of Biotechnology, HiLIFE, University of Helsinki, Helsinki, 00014</wicri:regionArea><orgName type="university">Université d'Helsinki</orgName><placeName><settlement type="city">Helsinki</settlement><region type="région" 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Sciences, Peking University, Beijing, 100871, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing, 100871</wicri:regionArea><orgName type="university">Université de Pékin</orgName><placeName><settlement type="city">Pékin</settlement><region type="capitale">Pékin</region></placeName></affiliation></author><author><name sortKey="Immanen, Juha" sort="Immanen, Juha" uniqKey="Immanen J" first="Juha" last="Immanen">Juha Immanen</name><affiliation wicri:level="4"><nlm:affiliation>Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, Viikki Plant Science Centre, University of Helsinki, Helsinki, 00014, Finland.</nlm:affiliation><country xml:lang="fr">Finlande</country><wicri:regionArea>Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental 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xml:lang="fr">Finlande</country><wicri:regionArea>Institute of Biotechnology, HiLIFE, University of Helsinki, Helsinki, 00014</wicri:regionArea><orgName type="university">Université d'Helsinki</orgName><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName></affiliation><affiliation wicri:level="4"><nlm:affiliation>Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, Viikki Plant Science Centre, University of Helsinki, Helsinki, 00014, Finland.</nlm:affiliation><country xml:lang="fr">Finlande</country><wicri:regionArea>Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, Viikki Plant Science Centre, University of Helsinki, Helsinki, 00014</wicri:regionArea><orgName type="university">Université d'Helsinki</orgName><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName></affiliation><affiliation wicri:level="4"><nlm:affiliation>The Sainsbury Laboratory, University of Cambridge, Bateman Street, Cambridge, CB2 1LR, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>The Sainsbury Laboratory, University of Cambridge, Bateman Street, Cambridge, CB2 1LR</wicri:regionArea><orgName type="university">Université de Cambridge</orgName><placeName><settlement type="city">Cambridge</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Angleterre de l'Est</region></placeName></affiliation></author><author><name sortKey="Zhang, Jing" sort="Zhang, Jing" uniqKey="Zhang J" first="Jing" last="Zhang">Jing Zhang</name><affiliation wicri:level="4"><nlm:affiliation>Institute of Biotechnology, HiLIFE, University of Helsinki, Helsinki, 00014, Finland.</nlm:affiliation><country xml:lang="fr">Finlande</country><wicri:regionArea>Institute of Biotechnology, HiLIFE, University of Helsinki, Helsinki, 00014</wicri:regionArea><orgName type="university">Université d'Helsinki</orgName><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName></affiliation><affiliation wicri:level="4"><nlm:affiliation>Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, Viikki Plant Science Centre, University of Helsinki, Helsinki, 00014, Finland.</nlm:affiliation><country xml:lang="fr">Finlande</country><wicri:regionArea>Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, Viikki Plant Science Centre, University of Helsinki, Helsinki, 00014</wicri:regionArea><orgName type="university">Université d'Helsinki</orgName><placeName><settlement type="city">Helsinki</settlement><region type="région" nuts="2">Uusimaa</region></placeName></affiliation></author><author><name sortKey="He, Xin Qiang" sort="He, Xin Qiang" uniqKey="He X" first="Xin-Qiang" last="He">Xin-Qiang He</name><affiliation wicri:level="4"><nlm:affiliation>State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing, 100871, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing, 100871</wicri:regionArea><orgName type="university">Université de Pékin</orgName><placeName><settlement type="city">Pékin</settlement><region type="capitale">Pékin</region></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>Cambium (physiology)</term><term>Cytokinins (metabolism)</term><term>Gene Expression Regulation, Plant (MeSH)</term><term>Genes, Plant (MeSH)</term><term>Indoleacetic Acids (metabolism)</term><term>Models, Biological (MeSH)</term><term>Phloem (physiology)</term><term>Plant Vascular Bundle (physiology)</term><term>Populus (genetics)</term><term>Populus (physiology)</term><term>Regeneration (physiology)</term><term>Trees (genetics)</term><term>Trees (physiology)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Acides indolacétiques (métabolisme)</term><term>Arbres (génétique)</term><term>Arbres (physiologie)</term><term>Cambium (physiologie)</term><term>Cytokinine (métabolisme)</term><term>Faisceau vasculaire des plantes (physiologie)</term><term>Gènes de plante (MeSH)</term><term>Modèles biologiques (MeSH)</term><term>Phloème (physiologie)</term><term>Populus (génétique)</term><term>Populus (physiologie)</term><term>Régulation de l'expression des gènes végétaux (MeSH)</term><term>Régénération (physiologie)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Cytokinins</term><term>Indoleacetic Acids</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Populus</term><term>Trees</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Arbres</term><term>Populus</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Acides indolacétiques</term><term>Cytokinine</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Arbres</term><term>Cambium</term><term>Faisceau vasculaire des plantes</term><term>Phloème</term><term>Populus</term><term>Régénération</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Cambium</term><term>Phloem</term><term>Plant Vascular Bundle</term><term>Populus</term><term>Regeneration</term><term>Trees</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Gene Expression Regulation, Plant</term><term>Genes, Plant</term><term>Models, Biological</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Gènes de plante</term><term>Modèles biologiques</term><term>Régulation de l'expression des gènes végétaux</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Tissue regeneration upon wounding in plants highlights the developmental plasticity of plants. Previous studies have described the morphological and molecular changes of secondary vascular tissue (SVT) regeneration after large-scale bark girdling in trees. However, how phytohormones regulate SVT regeneration is still unknown. Here, we established a novel in vitro SVT regeneration system in the hybrid aspen (Populus tremula × Populus tremuloides) clone T89 to bypass the limitation of using field-grown trees. The effects of phytohormones on SVT regeneration were investigated by applying exogenous hormones and utilizing various transgenic trees. Vascular tissue-specific markers and hormonal response factors were also examined during SVT regeneration. Using this in vitro regeneration system, we demonstrated that auxin and cytokinin differentially regulate phloem and cambium regeneration. Whereas auxin is sufficient to induce regeneration of phloem prior to continuous cambium restoration, cytokinin only promotes the formation of new phloem, not cambium. The positive role of cytokinin on phloem regeneration was further confirmed in cytokinin overexpression trees. Analysis of a DR5 reporter transgenic line further suggested that cytokinin blocks the re-establishment of auxin gradients, which is required for the cambium formation. Investigation on the auxin and cytokinin signalling genes indicated these two hormones interact to regulate SVT regeneration. Taken together, the in vitro SVT regeneration system allows us to make use of various molecular and genetic tools to investigate SVT regeneration. Our results confirmed that complementary auxin and cytokinin domains are required for phloem and cambium reconstruction.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">31230359</PMID><DateCompleted><Year>2020</Year><Month>05</Month><Day>04</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>224</Volume><Issue>1</Issue><PubDate><Year>2019</Year><Month>10</Month></PubDate></JournalIssue><Title>The New phytologist</Title><ISOAbbreviation>New Phytol</ISOAbbreviation></Journal><ArticleTitle>Differential regulation of auxin and cytokinin during the secondary vascular tissue regeneration in Populus trees.</ArticleTitle><Pagination><MedlinePgn>188-201</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.16019</ELocationID><Abstract><AbstractText>Tissue regeneration upon wounding in plants highlights the developmental plasticity of plants. Previous studies have described the morphological and molecular changes of secondary vascular tissue (SVT) regeneration after large-scale bark girdling in trees. However, how phytohormones regulate SVT regeneration is still unknown. Here, we established a novel in vitro SVT regeneration system in the hybrid aspen (Populus tremula × Populus tremuloides) clone T89 to bypass the limitation of using field-grown trees. The effects of phytohormones on SVT regeneration were investigated by applying exogenous hormones and utilizing various transgenic trees. Vascular tissue-specific markers and hormonal response factors were also examined during SVT regeneration. Using this in vitro regeneration system, we demonstrated that auxin and cytokinin differentially regulate phloem and cambium regeneration. Whereas auxin is sufficient to induce regeneration of phloem prior to continuous cambium restoration, cytokinin only promotes the formation of new phloem, not cambium. The positive role of cytokinin on phloem regeneration was further confirmed in cytokinin overexpression trees. Analysis of a DR5 reporter transgenic line further suggested that cytokinin blocks the re-establishment of auxin gradients, which is required for the cambium formation. Investigation on the auxin and cytokinin signalling genes indicated these two hormones interact to regulate SVT regeneration. Taken together, the in vitro SVT regeneration system allows us to make use of various molecular and genetic tools to investigate SVT regeneration. Our results confirmed that complementary auxin and cytokinin domains are required for phloem and cambium reconstruction.</AbstractText><CopyrightInformation>© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Jia-Jia</ForeName><Initials>JJ</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing, 100871, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Institute of Biotechnology, HiLIFE, University of Helsinki, Helsinki, 00014, Finland.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, Viikki Plant Science Centre, University of Helsinki, Helsinki, 00014, Finland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Ling-Yan</ForeName><Initials>LY</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing, 100871, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Immanen</LastName><ForeName>Juha</ForeName><Initials>J</Initials><Identifier Source="ORCID">0000-0003-1098-4843</Identifier><AffiliationInfo><Affiliation>Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, Viikki Plant Science Centre, University of Helsinki, Helsinki, 00014, Finland.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Natural Resources Institute Finland (Luke), Production Systems, Plant Genetics, Helsinki, 00790, Finland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nieminen</LastName><ForeName>Kaisa</ForeName><Initials>K</Initials><Identifier Source="ORCID">0000-0001-7004-9422</Identifier><AffiliationInfo><Affiliation>Natural Resources Institute Finland (Luke), Production Systems, Plant Genetics, Helsinki, 00790, Finland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Spicer</LastName><ForeName>Rachel</ForeName><Initials>R</Initials><Identifier Source="ORCID">0000-0002-1129-3932</Identifier><AffiliationInfo><Affiliation>Department of Botany, Connecticut College, New London, CT, 06320, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Helariutta</LastName><ForeName>Ykä</ForeName><Initials>Y</Initials><Identifier Source="ORCID">0000-0002-7287-8459</Identifier><AffiliationInfo><Affiliation>Institute of Biotechnology, HiLIFE, University of Helsinki, Helsinki, 00014, Finland.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, Viikki Plant Science Centre, University of Helsinki, Helsinki, 00014, Finland.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>The Sainsbury Laboratory, University of Cambridge, Bateman Street, Cambridge, CB2 1LR, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Jing</ForeName><Initials>J</Initials><Identifier Source="ORCID">0000-0003-4463-7516</Identifier><AffiliationInfo><Affiliation>Institute of Biotechnology, HiLIFE, University of Helsinki, Helsinki, 00014, Finland.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, Viikki Plant Science Centre, University of Helsinki, Helsinki, 00014, Finland.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>He</LastName><ForeName>Xin-Qiang</ForeName><Initials>XQ</Initials><Identifier Source="ORCID">0000-0002-1755-008X</Identifier><AffiliationInfo><Affiliation>State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing, 100871, China.</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></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>08</Month><Day>02</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="D003583">Cytokinins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D007210">Indoleacetic Acids</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D058506" MajorTopicYN="N">Cambium</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D003583" MajorTopicYN="N">Cytokinins</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D017343" MajorTopicYN="N">Genes, Plant</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D007210" MajorTopicYN="N">Indoleacetic Acids</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008954" MajorTopicYN="N">Models, Biological</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D052585" MajorTopicYN="N">Phloem</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D058526" MajorTopicYN="N">Plant Vascular Bundle</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D012038" MajorTopicYN="N">Regeneration</DescriptorName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D014197" MajorTopicYN="N">Trees</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Populus
</Keyword><Keyword MajorTopicYN="Y">auxin</Keyword><Keyword MajorTopicYN="Y">cambium</Keyword><Keyword MajorTopicYN="Y">cytokinin</Keyword><Keyword MajorTopicYN="Y">phloem</Keyword><Keyword MajorTopicYN="Y">vascular tissue regeneration</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>04</Month><Day>23</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>06</Month><Day>14</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>6</Month><Day>24</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>5</Month><Day>6</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>6</Month><Day>24</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">31230359</ArticleId><ArticleId IdType="doi">10.1111/nph.16019</ArticleId></ArticleIdList><ReferenceList><Title>References</Title><Reference><Citation>Agusti J, Lichtenberger R, Schwarz M, Nehlin L, Greb T. 2011. 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