A general model to explain repeated turnovers of sex determination in the Salicaceae.
Identifieur interne : 000067 ( Main/Corpus ); précédent : 000066; suivant : 000068A general model to explain repeated turnovers of sex determination in the Salicaceae.
Auteurs : Wenlu Yang ; Deyan Wang ; Yiling Li ; Zhiyang Zhang ; Shaofei Tong ; Mengmeng Li ; Xu Zhang ; Lei Zhang ; Liwen Ren ; Xinzhi Ma ; Ran Zhou ; Brian J. Sanderson ; Ken Keefover-Ring ; Tongming Yin ; Lawrence B. Smart ; Jianquan Liu ; Stephen P. Difazio ; Matthew Olson ; Tao MaSource :
- Molecular biology and evolution [ 1537-1719 ] ; 2020.
Abstract
Dioecy, the presence of separate sexes on distinct individuals, has evolved repeatedly in multiple plant lineages. However, the specific mechanisms by which sex systems evolve and their commonalities among plant species remain poorly understood. With both XY and ZW sex systems, the family Salicaceae provides a system to uncover the evolutionary forces driving sex chromosome turnovers. In this study, we performed a genome-wide association study to characterize sex determination in two Populus species, P. euphratica and P. alba. Our results reveal an XY system of sex determination on chromosome 14 of P. euphratica, and a ZW system on chromosome 19 of P. alba. We further assembled the corresponding sex determination regions, and found that their sex chromosome turnovers may be driven by the repeated translocations of a Helitron-like transposon. During the translocation, this factor may have captured partial or intact sequences that are orthologous to a type-A cytokinin response regulator gene. Based on results from this and other recently published studies, we hypothesize that this gene may act as a master regulator of sex determination for the entire family. We propose a general model to explain how the XY and ZW sex systems in this family can be determined by the same RR gene. Our study provides new insights into the diversification of incipient sex chromosomes in flowering plants by showing how transposition and rearrangement of a single gene can control sex in both XY and ZW systems.
DOI: 10.1093/molbev/msaa261
PubMed: 33027519
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Sanderson</name><affiliation><nlm:affiliation>Department of Biology, West Virginia University, Morgantown, WV, USA.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Department of Biological Sciences, Texas Tech University, Lubbock, TX USA.</nlm:affiliation></affiliation></author><author><name sortKey="Keefover Ring, Ken" sort="Keefover Ring, Ken" uniqKey="Keefover Ring K" first="Ken" last="Keefover-Ring">Ken Keefover-Ring</name><affiliation><nlm:affiliation>Departments of Botany and Geography, University of Wisconsin-Madison, 430 Lincoln Dr., Madison, WI, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Yin, Tongming" sort="Yin, Tongming" uniqKey="Yin T" first="Tongming" last="Yin">Tongming Yin</name><affiliation><nlm:affiliation>The Key Laboratory of Tree Genetics and Biotechnology of Jiangsu Province and Education Department of China, Nanjing Forestry University, Nanjing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Smart, Lawrence B" sort="Smart, Lawrence B" uniqKey="Smart L" first="Lawrence B" last="Smart">Lawrence B. Smart</name><affiliation><nlm:affiliation>Horticulture Section, School of Integrative Plant Science, Cornell University, New York State Agricultural Experiment Station, Geneva, New York, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Liu, Jianquan" sort="Liu, Jianquan" uniqKey="Liu J" first="Jianquan" last="Liu">Jianquan Liu</name><affiliation><nlm:affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>State Key Laboratory of Grassland Agro-Ecosystem, Institute of Innovation Ecology & College of Life Sciences, Lanzhou University, Lanzhou, China.</nlm:affiliation></affiliation></author><author><name sortKey="Difazio, Stephen P" sort="Difazio, Stephen P" uniqKey="Difazio S" first="Stephen P" last="Difazio">Stephen P. Difazio</name><affiliation><nlm:affiliation>Department of Biology, West Virginia University, Morgantown, WV, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Olson, Matthew" sort="Olson, Matthew" uniqKey="Olson M" first="Matthew" last="Olson">Matthew Olson</name><affiliation><nlm:affiliation>Department of Biological Sciences, Texas Tech University, Lubbock, TX USA.</nlm:affiliation></affiliation></author><author><name sortKey="Ma, Tao" sort="Ma, Tao" uniqKey="Ma T" first="Tao" last="Ma">Tao Ma</name><affiliation><nlm:affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:33027519</idno><idno type="pmid">33027519</idno><idno type="doi">10.1093/molbev/msaa261</idno><idno type="wicri:Area/Main/Corpus">000067</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000067</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">A general model to explain repeated turnovers of sex determination in the Salicaceae.</title><author><name sortKey="Yang, Wenlu" sort="Yang, Wenlu" uniqKey="Yang W" first="Wenlu" last="Yang">Wenlu Yang</name><affiliation><nlm:affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</nlm:affiliation></affiliation></author><author><name sortKey="Wang, Deyan" sort="Wang, Deyan" uniqKey="Wang D" first="Deyan" last="Wang">Deyan Wang</name><affiliation><nlm:affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</nlm:affiliation></affiliation></author><author><name sortKey="Li, Yiling" sort="Li, Yiling" uniqKey="Li Y" first="Yiling" last="Li">Yiling Li</name><affiliation><nlm:affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</nlm:affiliation></affiliation></author><author><name sortKey="Zhang, Zhiyang" sort="Zhang, Zhiyang" uniqKey="Zhang Z" first="Zhiyang" last="Zhang">Zhiyang Zhang</name><affiliation><nlm:affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</nlm:affiliation></affiliation></author><author><name sortKey="Tong, Shaofei" sort="Tong, Shaofei" uniqKey="Tong S" first="Shaofei" last="Tong">Shaofei Tong</name><affiliation><nlm:affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</nlm:affiliation></affiliation></author><author><name sortKey="Li, Mengmeng" sort="Li, Mengmeng" uniqKey="Li M" first="Mengmeng" last="Li">Mengmeng Li</name><affiliation><nlm:affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</nlm:affiliation></affiliation></author><author><name sortKey="Zhang, Xu" sort="Zhang, Xu" uniqKey="Zhang X" first="Xu" last="Zhang">Xu Zhang</name><affiliation><nlm:affiliation>State Key Laboratory of Grassland Agro-Ecosystem, Institute of Innovation Ecology & College of Life Sciences, Lanzhou University, Lanzhou, China.</nlm:affiliation></affiliation></author><author><name sortKey="Zhang, Lei" sort="Zhang, Lei" uniqKey="Zhang L" first="Lei" last="Zhang">Lei Zhang</name><affiliation><nlm:affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</nlm:affiliation></affiliation></author><author><name sortKey="Ren, Liwen" sort="Ren, Liwen" uniqKey="Ren L" first="Liwen" last="Ren">Liwen Ren</name><affiliation><nlm:affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</nlm:affiliation></affiliation></author><author><name sortKey="Ma, Xinzhi" sort="Ma, Xinzhi" uniqKey="Ma X" first="Xinzhi" last="Ma">Xinzhi Ma</name><affiliation><nlm:affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</nlm:affiliation></affiliation></author><author><name sortKey="Zhou, Ran" sort="Zhou, Ran" uniqKey="Zhou R" first="Ran" last="Zhou">Ran Zhou</name><affiliation><nlm:affiliation>Department of Biology, West Virginia University, Morgantown, WV, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Sanderson, Brian J" sort="Sanderson, Brian J" uniqKey="Sanderson B" first="Brian J" last="Sanderson">Brian J. Sanderson</name><affiliation><nlm:affiliation>Department of Biology, West Virginia University, Morgantown, WV, USA.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>Department of Biological Sciences, Texas Tech University, Lubbock, TX USA.</nlm:affiliation></affiliation></author><author><name sortKey="Keefover Ring, Ken" sort="Keefover Ring, Ken" uniqKey="Keefover Ring K" first="Ken" last="Keefover-Ring">Ken Keefover-Ring</name><affiliation><nlm:affiliation>Departments of Botany and Geography, University of Wisconsin-Madison, 430 Lincoln Dr., Madison, WI, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Yin, Tongming" sort="Yin, Tongming" uniqKey="Yin T" first="Tongming" last="Yin">Tongming Yin</name><affiliation><nlm:affiliation>The Key Laboratory of Tree Genetics and Biotechnology of Jiangsu Province and Education Department of China, Nanjing Forestry University, Nanjing, China.</nlm:affiliation></affiliation></author><author><name sortKey="Smart, Lawrence B" sort="Smart, Lawrence B" uniqKey="Smart L" first="Lawrence B" last="Smart">Lawrence B. Smart</name><affiliation><nlm:affiliation>Horticulture Section, School of Integrative Plant Science, Cornell University, New York State Agricultural Experiment Station, Geneva, New York, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Liu, Jianquan" sort="Liu, Jianquan" uniqKey="Liu J" first="Jianquan" last="Liu">Jianquan Liu</name><affiliation><nlm:affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</nlm:affiliation></affiliation><affiliation><nlm:affiliation>State Key Laboratory of Grassland Agro-Ecosystem, Institute of Innovation Ecology & College of Life Sciences, Lanzhou University, Lanzhou, China.</nlm:affiliation></affiliation></author><author><name sortKey="Difazio, Stephen P" sort="Difazio, Stephen P" uniqKey="Difazio S" first="Stephen P" last="Difazio">Stephen P. Difazio</name><affiliation><nlm:affiliation>Department of Biology, West Virginia University, Morgantown, WV, USA.</nlm:affiliation></affiliation></author><author><name sortKey="Olson, Matthew" sort="Olson, Matthew" uniqKey="Olson M" first="Matthew" last="Olson">Matthew Olson</name><affiliation><nlm:affiliation>Department of Biological Sciences, Texas Tech University, Lubbock, TX USA.</nlm:affiliation></affiliation></author><author><name sortKey="Ma, Tao" sort="Ma, Tao" uniqKey="Ma T" first="Tao" last="Ma">Tao Ma</name><affiliation><nlm:affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Molecular biology and evolution</title><idno type="eISSN">1537-1719</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">Dioecy, the presence of separate sexes on distinct individuals, has evolved repeatedly in multiple plant lineages. However, the specific mechanisms by which sex systems evolve and their commonalities among plant species remain poorly understood. With both XY and ZW sex systems, the family Salicaceae provides a system to uncover the evolutionary forces driving sex chromosome turnovers. In this study, we performed a genome-wide association study to characterize sex determination in two Populus species, P. euphratica and P. alba. Our results reveal an XY system of sex determination on chromosome 14 of P. euphratica, and a ZW system on chromosome 19 of P. alba. We further assembled the corresponding sex determination regions, and found that their sex chromosome turnovers may be driven by the repeated translocations of a Helitron-like transposon. During the translocation, this factor may have captured partial or intact sequences that are orthologous to a type-A cytokinin response regulator gene. Based on results from this and other recently published studies, we hypothesize that this gene may act as a master regulator of sex determination for the entire family. We propose a general model to explain how the XY and ZW sex systems in this family can be determined by the same RR gene. Our study provides new insights into the diversification of incipient sex chromosomes in flowering plants by showing how transposition and rearrangement of a single gene can control sex in both XY and ZW systems.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">33027519</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>07</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1537-1719</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Oct</Month><Day>07</Day></PubDate></JournalIssue><Title>Molecular biology and evolution</Title><ISOAbbreviation>Mol Biol Evol</ISOAbbreviation></Journal><ArticleTitle>A general model to explain repeated turnovers of sex determination in the Salicaceae.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">msaa261</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1093/molbev/msaa261</ELocationID><Abstract><AbstractText>Dioecy, the presence of separate sexes on distinct individuals, has evolved repeatedly in multiple plant lineages. However, the specific mechanisms by which sex systems evolve and their commonalities among plant species remain poorly understood. With both XY and ZW sex systems, the family Salicaceae provides a system to uncover the evolutionary forces driving sex chromosome turnovers. In this study, we performed a genome-wide association study to characterize sex determination in two Populus species, P. euphratica and P. alba. Our results reveal an XY system of sex determination on chromosome 14 of P. euphratica, and a ZW system on chromosome 19 of P. alba. We further assembled the corresponding sex determination regions, and found that their sex chromosome turnovers may be driven by the repeated translocations of a Helitron-like transposon. During the translocation, this factor may have captured partial or intact sequences that are orthologous to a type-A cytokinin response regulator gene. Based on results from this and other recently published studies, we hypothesize that this gene may act as a master regulator of sex determination for the entire family. We propose a general model to explain how the XY and ZW sex systems in this family can be determined by the same RR gene. Our study provides new insights into the diversification of incipient sex chromosomes in flowering plants by showing how transposition and rearrangement of a single gene can control sex in both XY and ZW systems.</AbstractText><CopyrightInformation>© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Yang</LastName><ForeName>Wenlu</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Deyan</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Yiling</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Zhiyang</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tong</LastName><ForeName>Shaofei</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Mengmeng</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Xu</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Grassland Agro-Ecosystem, Institute of Innovation Ecology & College of Life Sciences, Lanzhou University, Lanzhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Lei</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ren</LastName><ForeName>Liwen</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ma</LastName><ForeName>Xinzhi</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhou</LastName><ForeName>Ran</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Department of Biology, West Virginia University, Morgantown, WV, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sanderson</LastName><ForeName>Brian J</ForeName><Initials>BJ</Initials><AffiliationInfo><Affiliation>Department of Biology, West Virginia University, Morgantown, WV, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Biological Sciences, Texas Tech University, Lubbock, TX USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Keefover-Ring</LastName><ForeName>Ken</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Departments of Botany and Geography, University of Wisconsin-Madison, 430 Lincoln Dr., Madison, WI, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yin</LastName><ForeName>Tongming</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>The Key Laboratory of Tree Genetics and Biotechnology of Jiangsu Province and Education Department of China, Nanjing Forestry University, Nanjing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Smart</LastName><ForeName>Lawrence B</ForeName><Initials>LB</Initials><AffiliationInfo><Affiliation>Horticulture Section, School of Integrative Plant Science, Cornell University, New York State Agricultural Experiment Station, Geneva, New York, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Jianquan</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>State Key Laboratory of Grassland Agro-Ecosystem, Institute of Innovation Ecology & College of Life Sciences, Lanzhou University, Lanzhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>DiFazio</LastName><ForeName>Stephen P</ForeName><Initials>SP</Initials><AffiliationInfo><Affiliation>Department of Biology, West Virginia University, Morgantown, WV, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Olson</LastName><ForeName>Matthew</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Department of Biological Sciences, Texas Tech University, Lubbock, TX USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ma</LastName><ForeName>Tao</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>10</Month><Day>07</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Mol Biol Evol</MedlineTA><NlmUniqueID>8501455</NlmUniqueID><ISSNLinking>0737-4038</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Populus
</Keyword><Keyword MajorTopicYN="N">Dioecy</Keyword><Keyword MajorTopicYN="N">Genome</Keyword><Keyword MajorTopicYN="N">Sex chromosome turnover</Keyword><Keyword MajorTopicYN="N">Sex determination</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>04</Month><Day>30</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>08</Month><Day>18</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>09</Month><Day>29</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>10</Month><Day>7</Day><Hour>17</Hour><Minute>14</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>10</Month><Day>8</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>10</Month><Day>8</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">33027519</ArticleId><ArticleId IdType="pii">5919079</ArticleId><ArticleId IdType="doi">10.1093/molbev/msaa261</ArticleId></ArticleIdList></PubmedData></pubmed></record>Pour manipuler ce document sous Unix (Dilib)
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