Two nuclear effectors of the rice blast fungus modulate host immunity via transcriptional reprogramming.
Identifieur interne : 000012 ( Main/Exploration ); précédent : 000011; suivant : 000013Two nuclear effectors of the rice blast fungus modulate host immunity via transcriptional reprogramming.
Auteurs : Seongbeom Kim [Corée du Sud] ; Chi-Yeol Kim [Corée du Sud] ; Sook-Young Park [Corée du Sud] ; Ki-Tae Kim [Corée du Sud] ; Jongbum Jeon [Corée du Sud] ; Hyunjung Chung [Corée du Sud] ; Gobong Choi [Corée du Sud] ; Seomun Kwon [Corée du Sud, Allemagne] ; Jaeyoung Choi [Corée du Sud] ; Junhyun Jeon [Corée du Sud] ; Jong-Seong Jeon [Corée du Sud] ; Chang Hyun Khang [États-Unis] ; Seogchan Kang [États-Unis] ; Yong-Hwan Lee [Corée du Sud]Source :
- Nature communications [ 2041-1723 ] ; 2020.
Abstract
Pathogens utilize multiple types of effectors to modulate plant immunity. Although many apoplastic and cytoplasmic effectors have been reported, nuclear effectors have not been well characterized in fungal pathogens. Here, we characterize two nuclear effectors of the rice blast pathogen Magnaporthe oryzae. Both nuclear effectors are secreted via the biotrophic interfacial complex, translocated into the nuclei of initially penetrated and surrounding cells, and reprogram the expression of immunity-associated genes by binding on effector binding elements in rice. Their expression in transgenic rice causes ambivalent immunity: increased susceptibility to M. oryzae and Xanthomonas oryzae pv. oryzae, hemibiotrophic pathogens, but enhanced resistance to Cochliobolus miyabeanus, a necrotrophic pathogen. Our findings help remedy a significant knowledge deficiency in the mechanism of M. oryzae-rice interactions and underscore how effector-mediated manipulation of plant immunity by one pathogen may also affect the disease severity by other pathogens.
DOI: 10.1038/s41467-020-19624-w
PubMed: 33203871
Affiliations:
- Allemagne, Corée du Sud, États-Unis
- District de Düsseldorf, Pennsylvanie, Rhénanie-du-Nord-Westphalie
- Düsseldorf, Séoul, University Park (Pennsylvanie)
- Université d'État de Pennsylvanie, Université nationale de Séoul
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type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:33203871</idno><idno type="pmid">33203871</idno><idno type="doi">10.1038/s41467-020-19624-w</idno><idno type="wicri:Area/Main/Corpus">000006</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000006</idno><idno type="wicri:Area/Main/Curation">000006</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000006</idno><idno type="wicri:Area/Main/Exploration">000006</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Two nuclear effectors of the rice blast fungus modulate host immunity via transcriptional reprogramming.</title><author><name sortKey="Kim, Seongbeom" sort="Kim, Seongbeom" uniqKey="Kim S" first="Seongbeom" last="Kim">Seongbeom Kim</name><affiliation wicri:level="4"><nlm:affiliation>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826</wicri:regionArea><orgName type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation></author><author><name sortKey="Kim, Chi Yeol" sort="Kim, Chi Yeol" uniqKey="Kim C" first="Chi-Yeol" last="Kim">Chi-Yeol Kim</name><affiliation wicri:level="4"><nlm:affiliation>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826</wicri:regionArea><orgName type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation></author><author><name sortKey="Park, Sook Young" sort="Park, Sook Young" uniqKey="Park S" first="Sook-Young" last="Park">Sook-Young Park</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Medicine, Sunchon National University, Suncheon, 57922, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Plant Medicine, Sunchon National University, Suncheon, 57922</wicri:regionArea><wicri:noRegion>57922</wicri:noRegion></affiliation></author><author><name sortKey="Kim, Ki Tae" sort="Kim, Ki Tae" uniqKey="Kim K" first="Ki-Tae" last="Kim">Ki-Tae Kim</name><affiliation wicri:level="4"><nlm:affiliation>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826</wicri:regionArea><orgName type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation></author><author><name sortKey="Jeon, Jongbum" sort="Jeon, Jongbum" uniqKey="Jeon J" first="Jongbum" last="Jeon">Jongbum Jeon</name><affiliation wicri:level="4"><nlm:affiliation>Interdisciplinary Program in Agricultural Genomics, Seoul National University, Seoul, 08826, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Interdisciplinary Program in Agricultural Genomics, Seoul National University, Seoul, 08826</wicri:regionArea><orgName type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation></author><author><name sortKey="Chung, Hyunjung" sort="Chung, Hyunjung" uniqKey="Chung H" first="Hyunjung" last="Chung">Hyunjung Chung</name><affiliation wicri:level="4"><nlm:affiliation>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826</wicri:regionArea><orgName type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Crop Cultivation and Environment Research Division, National Institute of Crop Science, Rural Development Administration, Suwon, 16613, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Crop Cultivation and Environment Research Division, National Institute of Crop Science, Rural Development Administration, Suwon, 16613</wicri:regionArea><wicri:noRegion>16613</wicri:noRegion></affiliation></author><author><name sortKey="Choi, Gobong" sort="Choi, Gobong" uniqKey="Choi G" first="Gobong" last="Choi">Gobong Choi</name><affiliation wicri:level="4"><nlm:affiliation>Interdisciplinary Program in Agricultural Genomics, Seoul National University, Seoul, 08826, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Interdisciplinary Program in Agricultural Genomics, Seoul National University, Seoul, 08826</wicri:regionArea><orgName type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation></author><author><name sortKey="Kwon, Seomun" sort="Kwon, Seomun" uniqKey="Kwon S" first="Seomun" last="Kwon">Seomun Kwon</name><affiliation wicri:level="4"><nlm:affiliation>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826</wicri:regionArea><orgName type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Heinrich-Heine University Düsseldorf, Institute for Microbiology, Cluster of Excellence on Plant Sciences, Düsseldorf, 40204, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Heinrich-Heine University Düsseldorf, Institute for Microbiology, Cluster of Excellence on Plant Sciences, Düsseldorf, 40204</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Düsseldorf</region><settlement type="city">Düsseldorf</settlement></placeName></affiliation></author><author><name sortKey="Choi, Jaeyoung" sort="Choi, Jaeyoung" uniqKey="Choi J" first="Jaeyoung" last="Choi">Jaeyoung Choi</name><affiliation wicri:level="4"><nlm:affiliation>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826</wicri:regionArea><orgName type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Smart Farm Research Center, Korea Institute of Science and Technology, Gangneung, 25451, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Smart Farm Research Center, Korea Institute of Science and Technology, Gangneung, 25451</wicri:regionArea><wicri:noRegion>25451</wicri:noRegion></affiliation></author><author><name sortKey="Jeon, Junhyun" sort="Jeon, Junhyun" uniqKey="Jeon J" first="Junhyun" last="Jeon">Junhyun Jeon</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biotechnology, Yeungnam University, Gyeongsan, 38541, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Biotechnology, Yeungnam University, Gyeongsan, 38541</wicri:regionArea><wicri:noRegion>38541</wicri:noRegion></affiliation></author><author><name sortKey="Jeon, Jong Seong" sort="Jeon, Jong Seong" uniqKey="Jeon J" first="Jong-Seong" last="Jeon">Jong-Seong Jeon</name><affiliation wicri:level="1"><nlm:affiliation>Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University, Yongin, 17104, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University, Yongin, 17104</wicri:regionArea><wicri:noRegion>17104</wicri:noRegion></affiliation></author><author><name sortKey="Khang, Chang Hyun" sort="Khang, Chang Hyun" uniqKey="Khang C" first="Chang Hyun" last="Khang">Chang Hyun Khang</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Biology, University of Georgia, Athens, GA, 30602, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Biology, University of Georgia, Athens, GA, 30602</wicri:regionArea><wicri:noRegion>30602</wicri:noRegion></affiliation></author><author><name sortKey="Kang, Seogchan" sort="Kang, Seogchan" uniqKey="Kang S" first="Seogchan" last="Kang">Seogchan Kang</name><affiliation wicri:level="4"><nlm:affiliation>Department of Plant Pathology and Environmental Microbiology, The Pennsylvania State University, University Park, PA, 16802, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Pathology and Environmental Microbiology, The Pennsylvania State University, University Park, PA, 16802</wicri:regionArea><orgName type="university">Université d'État de Pennsylvanie</orgName><placeName><settlement type="city">University Park (Pennsylvanie)</settlement><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Lee, Yong Hwan" sort="Lee, Yong Hwan" uniqKey="Lee Y" first="Yong-Hwan" last="Lee">Yong-Hwan Lee</name><affiliation wicri:level="4"><nlm:affiliation>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826, Korea. yonglee@snu.ac.kr.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826</wicri:regionArea><orgName type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation><affiliation wicri:level="4"><nlm:affiliation>Interdisciplinary Program in Agricultural Genomics, Seoul National University, Seoul, 08826, Korea. yonglee@snu.ac.kr.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Interdisciplinary Program in Agricultural Genomics, Seoul National University, Seoul, 08826</wicri:regionArea><orgName type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation><affiliation wicri:level="4"><nlm:affiliation>Center for Fungal Genetic Resources, Plant Immunity Research Center, and Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul, 08826, Korea. yonglee@snu.ac.kr.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Center for Fungal Genetic Resources, Plant Immunity Research Center, and Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul, 08826</wicri:regionArea><orgName type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation></author></analytic><series><title level="j">Nature communications</title><idno type="eISSN">2041-1723</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">Pathogens utilize multiple types of effectors to modulate plant immunity. Although many apoplastic and cytoplasmic effectors have been reported, nuclear effectors have not been well characterized in fungal pathogens. Here, we characterize two nuclear effectors of the rice blast pathogen Magnaporthe oryzae. Both nuclear effectors are secreted via the biotrophic interfacial complex, translocated into the nuclei of initially penetrated and surrounding cells, and reprogram the expression of immunity-associated genes by binding on effector binding elements in rice. Their expression in transgenic rice causes ambivalent immunity: increased susceptibility to M. oryzae and Xanthomonas oryzae pv. oryzae, hemibiotrophic pathogens, but enhanced resistance to Cochliobolus miyabeanus, a necrotrophic pathogen. Our findings help remedy a significant knowledge deficiency in the mechanism of M. oryzae-rice interactions and underscore how effector-mediated manipulation of plant immunity by one pathogen may also affect the disease severity by other pathogens.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">33203871</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>18</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2041-1723</ISSN><JournalIssue CitedMedium="Internet"><Volume>11</Volume><Issue>1</Issue><PubDate><Year>2020</Year><Month>11</Month><Day>17</Day></PubDate></JournalIssue><Title>Nature communications</Title><ISOAbbreviation>Nat Commun</ISOAbbreviation></Journal><ArticleTitle>Two nuclear effectors of the rice blast fungus modulate host immunity via transcriptional reprogramming.</ArticleTitle><Pagination><MedlinePgn>5845</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1038/s41467-020-19624-w</ELocationID><Abstract><AbstractText>Pathogens utilize multiple types of effectors to modulate plant immunity. Although many apoplastic and cytoplasmic effectors have been reported, nuclear effectors have not been well characterized in fungal pathogens. Here, we characterize two nuclear effectors of the rice blast pathogen Magnaporthe oryzae. Both nuclear effectors are secreted via the biotrophic interfacial complex, translocated into the nuclei of initially penetrated and surrounding cells, and reprogram the expression of immunity-associated genes by binding on effector binding elements in rice. Their expression in transgenic rice causes ambivalent immunity: increased susceptibility to M. oryzae and Xanthomonas oryzae pv. oryzae, hemibiotrophic pathogens, but enhanced resistance to Cochliobolus miyabeanus, a necrotrophic pathogen. Our findings help remedy a significant knowledge deficiency in the mechanism of M. oryzae-rice interactions and underscore how effector-mediated manipulation of plant immunity by one pathogen may also affect the disease severity by other pathogens.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Kim</LastName><ForeName>Seongbeom</ForeName><Initials>S</Initials><Identifier Source="ORCID">0000-0003-0642-2303</Identifier><AffiliationInfo><Affiliation>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kim</LastName><ForeName>Chi-Yeol</ForeName><Initials>CY</Initials><AffiliationInfo><Affiliation>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Park</LastName><ForeName>Sook-Young</ForeName><Initials>SY</Initials><AffiliationInfo><Affiliation>Department of Plant Medicine, Sunchon National University, Suncheon, 57922, Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kim</LastName><ForeName>Ki-Tae</ForeName><Initials>KT</Initials><Identifier Source="ORCID">0000-0002-8249-5283</Identifier><AffiliationInfo><Affiliation>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jeon</LastName><ForeName>Jongbum</ForeName><Initials>J</Initials><Identifier Source="ORCID">0000-0003-3533-1363</Identifier><AffiliationInfo><Affiliation>Interdisciplinary Program in Agricultural Genomics, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chung</LastName><ForeName>Hyunjung</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Crop Cultivation and Environment Research Division, National Institute of Crop Science, Rural Development Administration, Suwon, 16613, Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Choi</LastName><ForeName>Gobong</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Interdisciplinary Program in Agricultural Genomics, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kwon</LastName><ForeName>Seomun</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Heinrich-Heine University Düsseldorf, Institute for Microbiology, Cluster of Excellence on Plant Sciences, Düsseldorf, 40204, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Choi</LastName><ForeName>Jaeyoung</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Smart Farm Research Center, Korea Institute of Science and Technology, Gangneung, 25451, Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jeon</LastName><ForeName>Junhyun</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Biotechnology, Yeungnam University, Gyeongsan, 38541, Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jeon</LastName><ForeName>Jong-Seong</ForeName><Initials>JS</Initials><Identifier Source="ORCID">0000-0001-6221-4993</Identifier><AffiliationInfo><Affiliation>Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University, Yongin, 17104, Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Khang</LastName><ForeName>Chang Hyun</ForeName><Initials>CH</Initials><AffiliationInfo><Affiliation>Department of Plant Biology, University of Georgia, Athens, GA, 30602, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kang</LastName><ForeName>Seogchan</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology and Environmental Microbiology, The Pennsylvania State University, University Park, PA, 16802, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lee</LastName><ForeName>Yong-Hwan</ForeName><Initials>YH</Initials><Identifier Source="ORCID">0000-0003-2462-1250</Identifier><AffiliationInfo><Affiliation>Department of Agricultural Biotechnology, Seoul National University, Seoul, 08826, Korea. yonglee@snu.ac.kr.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Interdisciplinary Program in Agricultural Genomics, Seoul National University, Seoul, 08826, Korea. yonglee@snu.ac.kr.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Center for Fungal Genetic Resources, Plant Immunity Research Center, and Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul, 08826, Korea. yonglee@snu.ac.kr.</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>2020</Year><Month>11</Month><Day>17</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Nat Commun</MedlineTA><NlmUniqueID>101528555</NlmUniqueID><ISSNLinking>2041-1723</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>05</Month><Day>07</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>10</Month><Day>20</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>11</Month><Day>18</Day><Hour>5</Hour><Minute>52</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>11</Month><Day>19</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>11</Month><Day>19</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">33203871</ArticleId><ArticleId IdType="doi">10.1038/s41467-020-19624-w</ArticleId><ArticleId IdType="pii">10.1038/s41467-020-19624-w</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Allemagne</li><li>Corée du Sud</li><li>États-Unis</li></country><region><li>District de Düsseldorf</li><li>Pennsylvanie</li><li>Rhénanie-du-Nord-Westphalie</li></region><settlement><li>Düsseldorf</li><li>Séoul</li><li>University Park (Pennsylvanie)</li></settlement><orgName><li>Université d'État de Pennsylvanie</li><li>Université nationale de Séoul</li></orgName></list><tree><country name="Corée du Sud"><noRegion><name sortKey="Kim, Seongbeom" sort="Kim, Seongbeom" uniqKey="Kim S" first="Seongbeom" last="Kim">Seongbeom Kim</name></noRegion><name sortKey="Choi, Gobong" sort="Choi, Gobong" uniqKey="Choi G" first="Gobong" last="Choi">Gobong Choi</name><name sortKey="Choi, Jaeyoung" sort="Choi, Jaeyoung" uniqKey="Choi J" first="Jaeyoung" last="Choi">Jaeyoung Choi</name><name sortKey="Choi, Jaeyoung" sort="Choi, Jaeyoung" uniqKey="Choi J" first="Jaeyoung" last="Choi">Jaeyoung Choi</name><name sortKey="Chung, Hyunjung" sort="Chung, Hyunjung" uniqKey="Chung H" first="Hyunjung" last="Chung">Hyunjung Chung</name><name sortKey="Chung, Hyunjung" sort="Chung, Hyunjung" uniqKey="Chung H" first="Hyunjung" last="Chung">Hyunjung Chung</name><name sortKey="Jeon, Jong Seong" sort="Jeon, Jong Seong" uniqKey="Jeon J" first="Jong-Seong" last="Jeon">Jong-Seong Jeon</name><name sortKey="Jeon, Jongbum" sort="Jeon, Jongbum" uniqKey="Jeon J" first="Jongbum" last="Jeon">Jongbum Jeon</name><name sortKey="Jeon, Junhyun" sort="Jeon, Junhyun" uniqKey="Jeon J" first="Junhyun" last="Jeon">Junhyun Jeon</name><name sortKey="Kim, Chi Yeol" sort="Kim, Chi Yeol" uniqKey="Kim C" first="Chi-Yeol" last="Kim">Chi-Yeol Kim</name><name sortKey="Kim, Ki Tae" sort="Kim, Ki Tae" uniqKey="Kim K" first="Ki-Tae" last="Kim">Ki-Tae Kim</name><name sortKey="Kwon, Seomun" sort="Kwon, Seomun" uniqKey="Kwon S" first="Seomun" last="Kwon">Seomun Kwon</name><name sortKey="Lee, Yong Hwan" sort="Lee, Yong Hwan" uniqKey="Lee Y" first="Yong-Hwan" last="Lee">Yong-Hwan Lee</name><name sortKey="Lee, Yong Hwan" sort="Lee, Yong Hwan" uniqKey="Lee Y" first="Yong-Hwan" last="Lee">Yong-Hwan Lee</name><name sortKey="Lee, Yong Hwan" sort="Lee, Yong Hwan" uniqKey="Lee Y" first="Yong-Hwan" last="Lee">Yong-Hwan Lee</name><name sortKey="Park, Sook Young" sort="Park, Sook Young" uniqKey="Park S" first="Sook-Young" last="Park">Sook-Young Park</name></country><country name="Allemagne"><region name="Rhénanie-du-Nord-Westphalie"><name sortKey="Kwon, Seomun" sort="Kwon, Seomun" uniqKey="Kwon S" first="Seomun" last="Kwon">Seomun Kwon</name></region></country><country name="États-Unis"><noRegion><name sortKey="Khang, Chang Hyun" sort="Khang, Chang Hyun" uniqKey="Khang C" first="Chang Hyun" last="Khang">Chang Hyun Khang</name></noRegion><name sortKey="Kang, Seogchan" sort="Kang, Seogchan" uniqKey="Kang S" first="Seogchan" last="Kang">Seogchan Kang</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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