Genome-wide identification of small G protein ROPs and their potential roles in Solanaceous family.
Identifieur interne : 000178 ( Main/Exploration ); précédent : 000177; suivant : 000179Genome-wide identification of small G protein ROPs and their potential roles in Solanaceous family.
Auteurs : Shuqing Yang [Pays-Bas] ; Ningning Yan [République populaire de Chine] ; Klaas Bouwmeester [Pays-Bas] ; Ren Na [République populaire de Chine] ; Zhiwei Zhang [République populaire de Chine] ; Jun Zhao [République populaire de Chine]Source :
- Gene [ 1879-0038 ] ; 2020.
Descripteurs français
- KwdFr :
- Capsicum (enzymologie), Capsicum (génétique), Génome végétal (MeSH), Maladies des plantes (génétique), Phylogenèse (MeSH), Protéines G monomériques (génétique), Protéines G monomériques (métabolisme), Protéines G rho (génétique), Protéines G rho (métabolisme), Protéines végétales (génétique), Protéines végétales (métabolisme), Solanaceae (enzymologie), Solanaceae (génétique), Tabac (enzymologie), Tabac (génétique), Transduction du signal (MeSH), Étude d'association pangénomique (méthodes).
- MESH :
- enzymologie : Capsicum, Solanaceae, Tabac.
- génétique : Capsicum, Maladies des plantes, Protéines G monomériques, Protéines G rho, Protéines végétales, Solanaceae, Tabac.
- métabolisme : Protéines G monomériques, Protéines G rho, Protéines végétales.
- méthodes : Étude d'association pangénomique.
- Génome végétal, Phylogenèse, Transduction du signal.
English descriptors
- KwdEn :
- Capsicum (enzymology), Capsicum (genetics), Genome, Plant (MeSH), Genome-Wide Association Study (methods), Monomeric GTP-Binding Proteins (genetics), Monomeric GTP-Binding Proteins (metabolism), Phylogeny (MeSH), Plant Diseases (genetics), Plant Proteins (genetics), Plant Proteins (metabolism), Signal Transduction (MeSH), Solanaceae (enzymology), Solanaceae (genetics), Tobacco (enzymology), Tobacco (genetics), rho GTP-Binding Proteins (genetics), rho GTP-Binding Proteins (metabolism).
- MESH :
- chemical , genetics : Monomeric GTP-Binding Proteins, Plant Proteins, rho GTP-Binding Proteins.
- enzymology : Capsicum, Solanaceae, Tobacco.
- genetics : Capsicum, Plant Diseases, Solanaceae, Tobacco.
- chemical , metabolism : Monomeric GTP-Binding Proteins, Plant Proteins, rho GTP-Binding Proteins.
- methods : Genome-Wide Association Study.
- Genome, Plant, Phylogeny, Signal Transduction.
Abstract
Small GTPases function as molecular switches to active or inactive signaling cascades via binding or hydrolyzing GTP. A type of plant specific small GTPases, the ROPs are known to be involved in plant growth, development and immunity. We determined whether ROPs are conserved in Solanaceous species and whether they are involved in plant growth, development and resistance against Phytophthora capsisi. In genome-wide screening, a total of 66 ROPs in six Solanaceous species (SolROPs) were identified, including 16 ROPs in Solanum tuberosum L. (potato), 9 in Solanum lycopersicum L. (tomato), 5 in Solanum melongena L. (eggplant), 9 in Capsicum annuum L. (pepper), 13 in Nicotiana benthamiana Domin and 14 in Nicotiana tabacum L. (tobacco). Phylogenetic analysis revealed that 11 AtROPs and 66 SolROPs fall into five distinct clades (I-V) and hence a novel and systematic gene nomenclature was proposed. In addition, a comprehensive expression analysis was performed by making use of an online database. This revealed that ROP genes are differentially expressed during plant growth and development. Moreover, gene expression of SlROP-II.1 in S. lycopersicum could be significantly induced by P. capsici. Subsequently, SlROP-II.1 and its homologues in N. benthamiana and C. annuum (NbROP-II.1 and CaROP-II.1) were selected for functional analysis using virus-induced gene silencing. Infection assays with P. capsici on silenced plants revealed that SlROP-II.1, NbROP-II.1 and CaROP-II.1 play a role in P. capsici resistance, suggesting conserved function of ROP-II clade across different Solanaceous species. In addition, NbROP-II.1 is also involved in regulating plant growth and development. This study signified the diversity of Solanaceous ROPs and their potential roles in plant growth, development and immunity.
DOI: 10.1016/j.gene.2020.144809
PubMed: 32470503
Affiliations:
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Electronic address: smartshuqing@outlook.com.</nlm:affiliation><country xml:lang="fr" wicri:curation="lc">Pays-Bas</country><wicri:regionArea>College of Horticulture and Plant Protection, Inner Mongolia Agricultural University, 010019 Hohhot, China; Vegetable Institute, Inner Mongolia Academy of Agriculture and Animal Husbandry Sciences, 010031 Hohhot, China; Laboratory of Phytopathology, Wageningen University and Research, 6708 PB Wageningen</wicri:regionArea><wicri:noRegion>6708 PB Wageningen</wicri:noRegion></affiliation></author><author><name sortKey="Yan, Ningning" sort="Yan, Ningning" uniqKey="Yan N" first="Ningning" last="Yan">Ningning Yan</name><affiliation wicri:level="1"><nlm:affiliation>College of Horticulture and Plant Protection, Inner Mongolia Agricultural University, 010019 Hohhot, China. Electronic address: 767252832@qq.com.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Horticulture and Plant Protection, Inner Mongolia Agricultural University, 010019 Hohhot</wicri:regionArea><wicri:noRegion>010019 Hohhot</wicri:noRegion></affiliation></author><author><name sortKey="Bouwmeester, Klaas" sort="Bouwmeester, Klaas" uniqKey="Bouwmeester K" first="Klaas" last="Bouwmeester">Klaas Bouwmeester</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Phytopathology, Wageningen University and Research, 6708 PB Wageningen, the Netherlands; Biosystematics Group, Wageningen University and Research, 6708 PB Wageningen, The Netherlands. Electronic address: klaas.bouwmeester@wur.nl.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Laboratory of Phytopathology, Wageningen University and Research, 6708 PB Wageningen, the Netherlands; Biosystematics Group, Wageningen University and Research, 6708 PB Wageningen</wicri:regionArea><wicri:noRegion>6708 PB Wageningen</wicri:noRegion></affiliation></author><author><name sortKey="Na, Ren" sort="Na, Ren" uniqKey="Na R" first="Ren" last="Na">Ren Na</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Cereal and Oil Crops, Hebei Academy of Agricultural and Forestry Sciences, 050035 Shijiazhuang, China. Electronic address: lnaren@hotmail.com.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Institute of Cereal and Oil Crops, Hebei Academy of Agricultural and Forestry Sciences, 050035 Shijiazhuang</wicri:regionArea><wicri:noRegion>050035 Shijiazhuang</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Zhiwei" sort="Zhang, Zhiwei" uniqKey="Zhang Z" first="Zhiwei" last="Zhang">Zhiwei Zhang</name><affiliation wicri:level="1"><nlm:affiliation>College of Horticulture and Plant Protection, Inner Mongolia Agricultural University, 010019 Hohhot, China. Electronic address: 276604636@qq.com.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Horticulture and Plant Protection, Inner Mongolia Agricultural University, 010019 Hohhot</wicri:regionArea><wicri:noRegion>010019 Hohhot</wicri:noRegion></affiliation></author><author><name sortKey="Zhao, Jun" sort="Zhao, Jun" uniqKey="Zhao J" first="Jun" last="Zhao">Jun Zhao</name><affiliation wicri:level="1"><nlm:affiliation>College of Horticulture and Plant Protection, Inner Mongolia Agricultural University, 010019 Hohhot, China. Electronic address: zhaojun@imau.edu.cn.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Horticulture and Plant Protection, Inner Mongolia Agricultural University, 010019 Hohhot</wicri:regionArea><wicri:noRegion>010019 Hohhot</wicri:noRegion></affiliation></author></analytic><series><title level="j">Gene</title><idno type="eISSN">1879-0038</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Capsicum (enzymology)</term><term>Capsicum (genetics)</term><term>Genome, Plant (MeSH)</term><term>Genome-Wide Association Study (methods)</term><term>Monomeric GTP-Binding Proteins (genetics)</term><term>Monomeric GTP-Binding Proteins (metabolism)</term><term>Phylogeny (MeSH)</term><term>Plant Diseases (genetics)</term><term>Plant Proteins (genetics)</term><term>Plant Proteins (metabolism)</term><term>Signal Transduction (MeSH)</term><term>Solanaceae (enzymology)</term><term>Solanaceae (genetics)</term><term>Tobacco (enzymology)</term><term>Tobacco (genetics)</term><term>rho GTP-Binding Proteins (genetics)</term><term>rho GTP-Binding Proteins (metabolism)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Capsicum (enzymologie)</term><term>Capsicum (génétique)</term><term>Génome végétal (MeSH)</term><term>Maladies des plantes (génétique)</term><term>Phylogenèse (MeSH)</term><term>Protéines G monomériques (génétique)</term><term>Protéines G monomériques (métabolisme)</term><term>Protéines G rho (génétique)</term><term>Protéines G rho (métabolisme)</term><term>Protéines végétales (génétique)</term><term>Protéines végétales (métabolisme)</term><term>Solanaceae (enzymologie)</term><term>Solanaceae (génétique)</term><term>Tabac (enzymologie)</term><term>Tabac (génétique)</term><term>Transduction du signal (MeSH)</term><term>Étude d'association pangénomique (méthodes)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Monomeric GTP-Binding Proteins</term><term>Plant Proteins</term><term>rho GTP-Binding Proteins</term></keywords><keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr"><term>Capsicum</term><term>Solanaceae</term><term>Tabac</term></keywords><keywords scheme="MESH" qualifier="enzymology" xml:lang="en"><term>Capsicum</term><term>Solanaceae</term><term>Tobacco</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Capsicum</term><term>Plant Diseases</term><term>Solanaceae</term><term>Tobacco</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Capsicum</term><term>Maladies des plantes</term><term>Protéines G monomériques</term><term>Protéines G rho</term><term>Protéines végétales</term><term>Solanaceae</term><term>Tabac</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Monomeric GTP-Binding Proteins</term><term>Plant Proteins</term><term>rho GTP-Binding Proteins</term></keywords><keywords scheme="MESH" qualifier="methods" xml:lang="en"><term>Genome-Wide Association Study</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Protéines G monomériques</term><term>Protéines G rho</term><term>Protéines végétales</term></keywords><keywords scheme="MESH" qualifier="méthodes" xml:lang="fr"><term>Étude d'association pangénomique</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Genome, Plant</term><term>Phylogeny</term><term>Signal Transduction</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Génome végétal</term><term>Phylogenèse</term><term>Transduction du signal</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Small GTPases function as molecular switches to active or inactive signaling cascades via binding or hydrolyzing GTP. A type of plant specific small GTPases, the ROPs are known to be involved in plant growth, development and immunity. We determined whether ROPs are conserved in Solanaceous species and whether they are involved in plant growth, development and resistance against Phytophthora capsisi. In genome-wide screening, a total of 66 ROPs in six Solanaceous species (SolROPs) were identified, including 16 ROPs in Solanum tuberosum L. (potato), 9 in Solanum lycopersicum L. (tomato), 5 in Solanum melongena L. (eggplant), 9 in Capsicum annuum L. (pepper), 13 in Nicotiana benthamiana Domin and 14 in Nicotiana tabacum L. (tobacco). Phylogenetic analysis revealed that 11 AtROPs and 66 SolROPs fall into five distinct clades (I-V) and hence a novel and systematic gene nomenclature was proposed. In addition, a comprehensive expression analysis was performed by making use of an online database. This revealed that ROP genes are differentially expressed during plant growth and development. Moreover, gene expression of SlROP-II.1 in S. lycopersicum could be significantly induced by P. capsici. Subsequently, SlROP-II.1 and its homologues in N. benthamiana and C. annuum (NbROP-II.1 and CaROP-II.1) were selected for functional analysis using virus-induced gene silencing. Infection assays with P. capsici on silenced plants revealed that SlROP-II.1, NbROP-II.1 and CaROP-II.1 play a role in P. capsici resistance, suggesting conserved function of ROP-II clade across different Solanaceous species. In addition, NbROP-II.1 is also involved in regulating plant growth and development. This study signified the diversity of Solanaceous ROPs and their potential roles in plant growth, development and immunity.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">32470503</PMID><DateCompleted><Year>2020</Year><Month>07</Month><Day>31</Day></DateCompleted><DateRevised><Year>2020</Year><Month>07</Month><Day>31</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1879-0038</ISSN><JournalIssue CitedMedium="Internet"><Volume>753</Volume><PubDate><Year>2020</Year><Month>Aug</Month><Day>30</Day></PubDate></JournalIssue><Title>Gene</Title><ISOAbbreviation>Gene</ISOAbbreviation></Journal><ArticleTitle>Genome-wide identification of small G protein ROPs and their potential roles in Solanaceous family.</ArticleTitle><Pagination><MedlinePgn>144809</MedlinePgn></Pagination><ELocationID EIdType="pii" ValidYN="Y">S0378-1119(20)30478-9</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1016/j.gene.2020.144809</ELocationID><Abstract><AbstractText>Small GTPases function as molecular switches to active or inactive signaling cascades via binding or hydrolyzing GTP. A type of plant specific small GTPases, the ROPs are known to be involved in plant growth, development and immunity. We determined whether ROPs are conserved in Solanaceous species and whether they are involved in plant growth, development and resistance against Phytophthora capsisi. In genome-wide screening, a total of 66 ROPs in six Solanaceous species (SolROPs) were identified, including 16 ROPs in Solanum tuberosum L. (potato), 9 in Solanum lycopersicum L. (tomato), 5 in Solanum melongena L. (eggplant), 9 in Capsicum annuum L. (pepper), 13 in Nicotiana benthamiana Domin and 14 in Nicotiana tabacum L. (tobacco). Phylogenetic analysis revealed that 11 AtROPs and 66 SolROPs fall into five distinct clades (I-V) and hence a novel and systematic gene nomenclature was proposed. In addition, a comprehensive expression analysis was performed by making use of an online database. This revealed that ROP genes are differentially expressed during plant growth and development. Moreover, gene expression of SlROP-II.1 in S. lycopersicum could be significantly induced by P. capsici. Subsequently, SlROP-II.1 and its homologues in N. benthamiana and C. annuum (NbROP-II.1 and CaROP-II.1) were selected for functional analysis using virus-induced gene silencing. Infection assays with P. capsici on silenced plants revealed that SlROP-II.1, NbROP-II.1 and CaROP-II.1 play a role in P. capsici resistance, suggesting conserved function of ROP-II clade across different Solanaceous species. In addition, NbROP-II.1 is also involved in regulating plant growth and development. This study signified the diversity of Solanaceous ROPs and their potential roles in plant growth, development and immunity.</AbstractText><CopyrightInformation>Copyright © 2020 Elsevier B.V. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Yang</LastName><ForeName>Shuqing</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>College of Horticulture and Plant Protection, Inner Mongolia Agricultural University, 010019 Hohhot, China; Vegetable Institute, Inner Mongolia Academy of Agriculture and Animal Husbandry Sciences, 010031 Hohhot, China; Laboratory of Phytopathology, Wageningen University and Research, 6708 PB Wageningen, the Netherlands. Electronic address: smartshuqing@outlook.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yan</LastName><ForeName>Ningning</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>College of Horticulture and Plant Protection, Inner Mongolia Agricultural University, 010019 Hohhot, China. Electronic address: 767252832@qq.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bouwmeester</LastName><ForeName>Klaas</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Laboratory of Phytopathology, Wageningen University and Research, 6708 PB Wageningen, the Netherlands; Biosystematics Group, Wageningen University and Research, 6708 PB Wageningen, The Netherlands. Electronic address: klaas.bouwmeester@wur.nl.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Na</LastName><ForeName>Ren</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Institute of Cereal and Oil Crops, Hebei Academy of Agricultural and Forestry Sciences, 050035 Shijiazhuang, China. Electronic address: lnaren@hotmail.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Zhiwei</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>College of Horticulture and Plant Protection, Inner Mongolia Agricultural University, 010019 Hohhot, China. Electronic address: 276604636@qq.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhao</LastName><ForeName>Jun</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>College of Horticulture and Plant Protection, Inner Mongolia Agricultural University, 010019 Hohhot, China. Electronic address: zhaojun@imau.edu.cn.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>05</Month><Day>26</Day></ArticleDate></Article><MedlineJournalInfo><Country>Netherlands</Country><MedlineTA>Gene</MedlineTA><NlmUniqueID>7706761</NlmUniqueID><ISSNLinking>0378-1119</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 3.6.5.2</RegistryNumber><NameOfSubstance UI="D020559">Monomeric GTP-Binding Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 3.6.5.2</RegistryNumber><NameOfSubstance UI="D020741">rho GTP-Binding Proteins</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D002212" MajorTopicYN="N">Capsicum</DescriptorName><QualifierName UI="Q000201" MajorTopicYN="N">enzymology</QualifierName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D018745" MajorTopicYN="N">Genome, Plant</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D055106" MajorTopicYN="N">Genome-Wide Association Study</DescriptorName><QualifierName UI="Q000379" MajorTopicYN="N">methods</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D020559" MajorTopicYN="N">Monomeric GTP-Binding Proteins</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010802" MajorTopicYN="N">Phylogeny</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D015398" MajorTopicYN="N">Signal Transduction</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D019657" MajorTopicYN="N">Solanaceae</DescriptorName><QualifierName UI="Q000201" MajorTopicYN="Y">enzymology</QualifierName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D014026" MajorTopicYN="N">Tobacco</DescriptorName><QualifierName UI="Q000201" MajorTopicYN="N">enzymology</QualifierName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D020741" MajorTopicYN="N">rho GTP-Binding Proteins</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Genome-wide screening</Keyword><Keyword MajorTopicYN="N">Phylogenetic analysis</Keyword><Keyword MajorTopicYN="N">Plant growth and development</Keyword><Keyword MajorTopicYN="N">Plant immunity</Keyword><Keyword MajorTopicYN="N">Small GTPase ROPs</Keyword><Keyword MajorTopicYN="N">Solanaceous family</Keyword></KeywordList><CoiStatement>Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>03</Month><Day>20</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>05</Month><Day>20</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>05</Month><Day>22</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>5</Month><Day>30</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>8</Month><Day>1</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>5</Month><Day>30</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32470503</ArticleId><ArticleId IdType="pii">S0378-1119(20)30478-9</ArticleId><ArticleId IdType="doi">10.1016/j.gene.2020.144809</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Pays-Bas</li><li>République populaire de Chine</li></country></list><tree><country name="Pays-Bas"><noRegion><name sortKey="Yang, Shuqing" sort="Yang, Shuqing" uniqKey="Yang S" first="Shuqing" last="Yang">Shuqing Yang</name></noRegion><name sortKey="Bouwmeester, Klaas" sort="Bouwmeester, Klaas" uniqKey="Bouwmeester K" first="Klaas" last="Bouwmeester">Klaas Bouwmeester</name></country><country name="République populaire de Chine"><noRegion><name sortKey="Yan, Ningning" sort="Yan, Ningning" uniqKey="Yan N" first="Ningning" last="Yan">Ningning Yan</name></noRegion><name sortKey="Na, Ren" sort="Na, Ren" uniqKey="Na R" first="Ren" last="Na">Ren Na</name><name sortKey="Zhang, Zhiwei" sort="Zhang, Zhiwei" uniqKey="Zhang Z" first="Zhiwei" last="Zhang">Zhiwei Zhang</name><name sortKey="Zhao, Jun" sort="Zhao, Jun" uniqKey="Zhao J" first="Jun" last="Zhao">Jun Zhao</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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