Linkage-linkage disequilibrium dissection of the epigenetic quantitative trait loci (epiQTLs) underlying growth and wood properties in Populus.
Identifieur interne : 000288 ( Main/Exploration ); précédent : 000287; suivant : 000289Linkage-linkage disequilibrium dissection of the epigenetic quantitative trait loci (epiQTLs) underlying growth and wood properties in Populus.
Auteurs : Wenjie Lu [République populaire de Chine] ; Liang Xiao [République populaire de Chine] ; Mingyang Quan [République populaire de Chine] ; Qingshi Wang [République populaire de Chine] ; Yousry A. El-Kassaby [Canada] ; Qingzhang Du [République populaire de Chine] ; Deqiang Zhang [République populaire de Chine]Source :
- The New phytologist [ 1469-8137 ] ; 2020.
Abstract
Increasing evidence indicates that DNA methylation is heritable and serves as an essential marker contributing to phenotypic variation. Linkage-linkage disequilibrium mapping was used to decipher the epigenetic architecture underlying nine growth and wood property traits in a linkage population (550 F1 progeny) and a natural population (435 unrelated individuals) of Populus using methylation-sensitive amplification polymorphism (MSAP)-based analysis. The interactions between genetic and epigenetic variants in the causative genes was further unveiled using expression quantitative trait methylation (eQTM) and nucleotide (eQTN) mapping strategies. A total of 163 epigenetic quantitative trait loci (epiQTLs; LOD ≥ 3.0), explaining 1.7-44.5% of phenotypic variations, were mapped to a high-resolution epigenetic map with 19 linkage groups, which was supported by the significant MSAP associations (P < 0.001) in the two populations. There were 23 causal genes involved in growth regulation and wood formation, whose markers were located in epiQTLs and associated with the same traits in both populations. Further eQTN and eQTM mapping showed that causal genetic and epigenetic variants within the 23 candidate genes may interact more in trans in gene expression and phenotype. The present study provides strategies for investigating epigenetic architecture and the interaction between genetic and epigenetic variants modulating complex traits in forest trees.
DOI: 10.1111/nph.16220
PubMed: 31560799
Affiliations:
- Canada, République populaire de Chine
- Colombie-Britannique
- Pékin, Vancouver
- Université de la Colombie-Britannique
Links toward previous steps (curation, corpus...)
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China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Xiao, Liang" sort="Xiao, Liang" uniqKey="Xiao L" first="Liang" last="Xiao">Liang Xiao</name><affiliation wicri:level="1"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation><affiliation wicri:level="3"><nlm:affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Quan, Mingyang" sort="Quan, Mingyang" uniqKey="Quan M" first="Mingyang" last="Quan">Mingyang Quan</name><affiliation wicri:level="1"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation><affiliation wicri:level="3"><nlm:affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Wang, Qingshi" sort="Wang, Qingshi" uniqKey="Wang Q" first="Qingshi" last="Wang">Qingshi Wang</name><affiliation wicri:level="1"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation><affiliation wicri:level="3"><nlm:affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="El Kassaby, Yousry A" sort="El Kassaby, Yousry A" uniqKey="El Kassaby Y" first="Yousry A" last="El-Kassaby">Yousry A. El-Kassaby</name><affiliation wicri:level="4"><nlm:affiliation>Department of Forest and Conservation Sciences, Faculty of Forestry, Forest Sciences Centre, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Department of Forest and Conservation Sciences, Faculty of Forestry, Forest Sciences Centre, University of British Columbia, Vancouver, BC, V6T 1Z4</wicri:regionArea><orgName type="university">Université de la Colombie-Britannique</orgName><placeName><settlement type="city">Vancouver</settlement><region type="state">Colombie-Britannique </region></placeName></affiliation></author><author><name sortKey="Du, Qingzhang" sort="Du, Qingzhang" uniqKey="Du Q" first="Qingzhang" last="Du">Qingzhang Du</name><affiliation wicri:level="1"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation><affiliation wicri:level="3"><nlm:affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Zhang, Deqiang" sort="Zhang, Deqiang" uniqKey="Zhang D" first="Deqiang" last="Zhang">Deqiang Zhang</name><affiliation wicri:level="1"><nlm:affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083</wicri:regionArea><wicri:noRegion>100083</wicri:noRegion></affiliation><affiliation wicri:level="3"><nlm:affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author></analytic><series><title level="j">The New phytologist</title><idno type="eISSN">1469-8137</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Increasing evidence indicates that DNA methylation is heritable and serves as an essential marker contributing to phenotypic variation. Linkage-linkage disequilibrium mapping was used to decipher the epigenetic architecture underlying nine growth and wood property traits in a linkage population (550 F<sub>1</sub> progeny) and a natural population (435 unrelated individuals) of Populus using methylation-sensitive amplification polymorphism (MSAP)-based analysis. The interactions between genetic and epigenetic variants in the causative genes was further unveiled using expression quantitative trait methylation (eQTM) and nucleotide (eQTN) mapping strategies. A total of 163 epigenetic quantitative trait loci (epiQTLs; LOD ≥ 3.0), explaining 1.7-44.5% of phenotypic variations, were mapped to a high-resolution epigenetic map with 19 linkage groups, which was supported by the significant MSAP associations (P < 0.001) in the two populations. There were 23 causal genes involved in growth regulation and wood formation, whose markers were located in epiQTLs and associated with the same traits in both populations. Further eQTN and eQTM mapping showed that causal genetic and epigenetic variants within the 23 candidate genes may interact more in trans in gene expression and phenotype. The present study provides strategies for investigating epigenetic architecture and the interaction between genetic and epigenetic variants modulating complex traits in forest trees.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">31560799</PMID><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>225</Volume><Issue>3</Issue><PubDate><Year>2020</Year><Month>02</Month></PubDate></JournalIssue><Title>The New phytologist</Title><ISOAbbreviation>New Phytol</ISOAbbreviation></Journal><ArticleTitle>Linkage-linkage disequilibrium dissection of the epigenetic quantitative trait loci (epiQTLs) underlying growth and wood properties in Populus.</ArticleTitle><Pagination><MedlinePgn>1218-1233</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.16220</ELocationID><Abstract><AbstractText>Increasing evidence indicates that DNA methylation is heritable and serves as an essential marker contributing to phenotypic variation. Linkage-linkage disequilibrium mapping was used to decipher the epigenetic architecture underlying nine growth and wood property traits in a linkage population (550 F<sub>1</sub> progeny) and a natural population (435 unrelated individuals) of Populus using methylation-sensitive amplification polymorphism (MSAP)-based analysis. The interactions between genetic and epigenetic variants in the causative genes was further unveiled using expression quantitative trait methylation (eQTM) and nucleotide (eQTN) mapping strategies. A total of 163 epigenetic quantitative trait loci (epiQTLs; LOD ≥ 3.0), explaining 1.7-44.5% of phenotypic variations, were mapped to a high-resolution epigenetic map with 19 linkage groups, which was supported by the significant MSAP associations (P < 0.001) in the two populations. There were 23 causal genes involved in growth regulation and wood formation, whose markers were located in epiQTLs and associated with the same traits in both populations. Further eQTN and eQTM mapping showed that causal genetic and epigenetic variants within the 23 candidate genes may interact more in trans in gene expression and phenotype. The present study provides strategies for investigating epigenetic architecture and the interaction between genetic and epigenetic variants modulating complex traits in forest trees.</AbstractText><CopyrightInformation>© 2019 The Authors New Phytologist © 2019 New Phytologist Trust.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Lu</LastName><ForeName>Wenjie</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xiao</LastName><ForeName>Liang</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Quan</LastName><ForeName>Mingyang</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Qingshi</ForeName><Initials>Q</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>El-Kassaby</LastName><ForeName>Yousry A</ForeName><Initials>YA</Initials><AffiliationInfo><Affiliation>Department of Forest and Conservation Sciences, Faculty of Forestry, Forest Sciences Centre, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Du</LastName><ForeName>Qingzhang</ForeName><Initials>Q</Initials><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Deqiang</ForeName><Initials>D</Initials><Identifier Source="ORCID">0000-0002-8849-2366</Identifier><AffiliationInfo><Affiliation>Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, 35 Qinghua East Road, Beijing, 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>11</Month><Day>01</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>New Phytol</MedlineTA><NlmUniqueID>9882884</NlmUniqueID><ISSNLinking>0028-646X</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Populus
</Keyword><Keyword MajorTopicYN="Y">association genetics</Keyword><Keyword MajorTopicYN="Y">eQTM</Keyword><Keyword MajorTopicYN="Y">eQTN</Keyword><Keyword MajorTopicYN="Y">epiQTL</Keyword><Keyword MajorTopicYN="Y">epigenetic map</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>06</Month><Day>07</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>09</Month><Day>17</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>9</Month><Day>29</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2019</Year><Month>9</Month><Day>29</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>9</Month><Day>28</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">31560799</ArticleId><ArticleId IdType="doi">10.1111/nph.16220</ArticleId></ArticleIdList><ReferenceList><Title>References</Title><Reference><Citation>Becker C, Hagmann J, Müller J, Koenig D, Stegle O, Borgwardt K, Weigel D. 2011. 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HfdIndexSelect -h $EXPLOR_AREA/Data/Main/Exploration/RBID.i -Sk "pubmed:31560799" \
| HfdSelect -Kh $EXPLOR_AREA/Data/Main/Exploration/biblio.hfd \
| NlmPubMed2Wicri -a PoplarV1
| This area was generated with Dilib version V0.6.37. |  |