A VASt-domain protein regulates autophagy, membrane tension, and sterol homeostasis in rice blast fungus.
Identifieur interne : 000160 ( Main/Exploration ); précédent : 000159; suivant : 000161A VASt-domain protein regulates autophagy, membrane tension, and sterol homeostasis in rice blast fungus.
Auteurs : Xue-Ming Zhu [République populaire de Chine] ; Lin Li [République populaire de Chine] ; Ying-Ying Cai [République populaire de Chine] ; Xi-Yu Wu [République populaire de Chine] ; Huan-Bin Shi [République populaire de Chine] ; Shuang Liang [République populaire de Chine] ; Ying-Min Qu [République populaire de Chine] ; Naweed I. Naqvi ; Maurizio Del Poeta [États-Unis] ; Bo Dong [États-Unis] ; Fu-Cheng Lin [République populaire de Chine] ; Xiao-Hong Liu [République populaire de Chine]Source :
- Autophagy [ 1554-8635 ] ; 2020.
Abstract
Sterols are a class of lipids critical for fundamental biological processes and membrane dynamics. These molecules are synthesized in the endoplasmic reticulum (ER) and are transported bi-directionally between the ER and plasma membrane (PM). However, the trafficking mechanism of sterols and their relationship with macroautophagy/autophagy are still poorly understood in the rice blast fungus Magnaporthe oryzae. Here, we identified the VAD1 Analog of StAR-related lipid transfer (VASt) domain-containing protein MoVast1 via co-immunoprecipitation in M. oryzae. Loss of MoVAST1 resulted in conidial defects, impaired appressorium development, and reduced pathogenicity. The MoTor (target of rapamycin in M. oryzae) activity is inhibited because MoVast1 deletion leads to high levels of sterol accumulation in the PM. Site-directed mutagenesis showed that the 902T site is essential for localization and function of MoVast1. Through filipin or Flipper-TR staining, autophagic flux detection, MoAtg8 lipidation, and drug sensitivity assays, we uncovered that MoVast1 acts as a novel autophagy inhibition factor that monitors tension in the PM by regulating the sterol content, which in turn modulates the activity of MoTor. Lipidomics and transcriptomics analyses further confirmed that MoVast1 is an important regulator of lipid metabolism and the autophagy pathway. Our results revealed and characterized a novel sterol transfer protein important for M. oryzae pathogenicity.
DOI: 10.1080/15548627.2020.1848129
PubMed: 33176558
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xml:lang="en">A VASt-domain protein regulates autophagy, membrane tension, and sterol homeostasis in rice blast fungus.</title><author><name sortKey="Zhu, Xue Ming" sort="Zhu, Xue Ming" uniqKey="Zhu X" first="Xue-Ming" last="Zhu">Xue-Ming Zhu</name><affiliation wicri:level="1"><nlm:affiliation>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058</wicri:regionArea><placeName><settlement type="city">Hangzhou</settlement><region type="province">Zhejiang</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences , Hangzhou 310021, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences , Hangzhou 310021</wicri:regionArea><placeName><settlement type="city">Hangzhou</settlement><region type="province">Zhejiang</region></placeName></affiliation></author><author><name sortKey="Li, Lin" sort="Li, Lin" uniqKey="Li L" first="Lin" last="Li">Lin Li</name><affiliation wicri:level="1"><nlm:affiliation>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058</wicri:regionArea><placeName><settlement type="city">Hangzhou</settlement><region type="province">Zhejiang</region></placeName></affiliation></author><author><name sortKey="Cai, Ying Ying" sort="Cai, Ying Ying" uniqKey="Cai Y" first="Ying-Ying" last="Cai">Ying-Ying Cai</name><affiliation wicri:level="1"><nlm:affiliation>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058</wicri:regionArea><placeName><settlement type="city">Hangzhou</settlement><region type="province">Zhejiang</region></placeName></affiliation></author><author><name sortKey="Wu, Xi Yu" sort="Wu, Xi Yu" uniqKey="Wu X" first="Xi-Yu" last="Wu">Xi-Yu Wu</name><affiliation wicri:level="1"><nlm:affiliation>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058</wicri:regionArea><placeName><settlement type="city">Hangzhou</settlement><region type="province">Zhejiang</region></placeName></affiliation></author><author><name sortKey="Shi, Huan Bin" sort="Shi, Huan Bin" uniqKey="Shi H" first="Huan-Bin" last="Shi">Huan-Bin Shi</name><affiliation wicri:level="1"><nlm:affiliation>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058</wicri:regionArea><placeName><settlement type="city">Hangzhou</settlement><region type="province">Zhejiang</region></placeName></affiliation></author><author><name sortKey="Liang, Shuang" sort="Liang, Shuang" uniqKey="Liang S" first="Shuang" last="Liang">Shuang Liang</name><affiliation wicri:level="1"><nlm:affiliation>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058</wicri:regionArea><placeName><settlement type="city">Hangzhou</settlement><region type="province">Zhejiang</region></placeName></affiliation></author><author><name sortKey="Qu, Ying Min" sort="Qu, Ying Min" uniqKey="Qu Y" first="Ying-Min" last="Qu">Ying-Min Qu</name><affiliation wicri:level="1"><nlm:affiliation>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058</wicri:regionArea><placeName><settlement type="city">Hangzhou</settlement><region type="province">Zhejiang</region></placeName></affiliation></author><author><name sortKey="Naqvi, Naweed I" sort="Naqvi, Naweed I" uniqKey="Naqvi N" first="Naweed I" last="Naqvi">Naweed I. Naqvi</name><affiliation><nlm:affiliation>Temasek Life Sciences Laboratory, Department of Biological Sciences, National University of Singapore , Singapore 117604.</nlm:affiliation><wicri:noCountry code="subField">Singapore 117604</wicri:noCountry></affiliation></author><author><name sortKey="Del Poeta, Maurizio" sort="Del Poeta, Maurizio" uniqKey="Del Poeta M" first="Maurizio" last="Del Poeta">Maurizio Del Poeta</name><affiliation wicri:level="2"><nlm:affiliation>Department of Microbiology and Immunology, Stony Brook University , Stony Brook, New York, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, Stony Brook University , Stony Brook, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Division of Infectious Diseases, Stony Brook University , Stony Brook, New York, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Infectious Diseases, Stony Brook University , Stony Brook, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Veterans Affairs Medical Center , Northport, New York, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Veterans Affairs Medical Center , Northport, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Dong, Bo" sort="Dong, Bo" uniqKey="Dong B" first="Bo" last="Dong">Bo Dong</name><affiliation wicri:level="2"><nlm:affiliation>Markey Cancer Center, University of Kentucky, College of Medicine , Lexington, KY 40506, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Markey Cancer Center, University of Kentucky, College of Medicine , Lexington, KY 40506</wicri:regionArea><placeName><region type="state">Kentucky</region></placeName></affiliation></author><author><name sortKey="Lin, Fu Cheng" sort="Lin, Fu Cheng" uniqKey="Lin F" first="Fu-Cheng" last="Lin">Fu-Cheng Lin</name><affiliation wicri:level="1"><nlm:affiliation>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058</wicri:regionArea><placeName><settlement type="city">Hangzhou</settlement><region type="province">Zhejiang</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences , Hangzhou 310021, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences , Hangzhou 310021</wicri:regionArea><placeName><settlement type="city">Hangzhou</settlement><region type="province">Zhejiang</region></placeName></affiliation></author><author><name sortKey="Liu, Xiao Hong" sort="Liu, Xiao Hong" uniqKey="Liu X" first="Xiao-Hong" last="Liu">Xiao-Hong Liu</name><affiliation wicri:level="1"><nlm:affiliation>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058</wicri:regionArea><placeName><settlement type="city">Hangzhou</settlement><region type="province">Zhejiang</region></placeName></affiliation></author></analytic><series><title level="j">Autophagy</title><idno type="eISSN">1554-8635</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">Sterols are a class of lipids critical for fundamental biological processes and membrane dynamics. These molecules are synthesized in the endoplasmic reticulum (ER) and are transported bi-directionally between the ER and plasma membrane (PM). However, the trafficking mechanism of sterols and their relationship with macroautophagy/autophagy are still poorly understood in the rice blast fungus <i>Magnaporthe oryzae</i>. Here, we identified the VAD1 Analog of StAR-related lipid transfer (VASt) domain-containing protein MoVast1 via co-immunoprecipitation in <i>M. oryzae</i>. Loss of <i>MoVAST1</i> resulted in conidial defects, impaired appressorium development, and reduced pathogenicity. The MoTor (target of rapamycin in <i>M. oryzae</i>) activity is inhibited because MoVast1 deletion leads to high levels of sterol accumulation in the PM. Site-directed mutagenesis showed that the 902T site is essential for localization and function of MoVast1. Through filipin or Flipper-TR staining, autophagic flux detection, MoAtg8 lipidation, and drug sensitivity assays, we uncovered that MoVast1 acts as a novel autophagy inhibition factor that monitors tension in the PM by regulating the sterol content, which in turn modulates the activity of MoTor. Lipidomics and transcriptomics analyses further confirmed that MoVast1 is an important regulator of lipid metabolism and the autophagy pathway. Our results revealed and characterized a novel sterol transfer protein important for <i>M. oryzae</i> pathogenicity.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">33176558</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>12</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1554-8635</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Nov</Month><Day>11</Day></PubDate></JournalIssue><Title>Autophagy</Title><ISOAbbreviation>Autophagy</ISOAbbreviation></Journal><ArticleTitle>A VASt-domain protein regulates autophagy, membrane tension, and sterol homeostasis in rice blast fungus.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1080/15548627.2020.1848129</ELocationID><Abstract><AbstractText>Sterols are a class of lipids critical for fundamental biological processes and membrane dynamics. These molecules are synthesized in the endoplasmic reticulum (ER) and are transported bi-directionally between the ER and plasma membrane (PM). However, the trafficking mechanism of sterols and their relationship with macroautophagy/autophagy are still poorly understood in the rice blast fungus <i>Magnaporthe oryzae</i>. Here, we identified the VAD1 Analog of StAR-related lipid transfer (VASt) domain-containing protein MoVast1 via co-immunoprecipitation in <i>M. oryzae</i>. Loss of <i>MoVAST1</i> resulted in conidial defects, impaired appressorium development, and reduced pathogenicity. The MoTor (target of rapamycin in <i>M. oryzae</i>) activity is inhibited because MoVast1 deletion leads to high levels of sterol accumulation in the PM. Site-directed mutagenesis showed that the 902T site is essential for localization and function of MoVast1. Through filipin or Flipper-TR staining, autophagic flux detection, MoAtg8 lipidation, and drug sensitivity assays, we uncovered that MoVast1 acts as a novel autophagy inhibition factor that monitors tension in the PM by regulating the sterol content, which in turn modulates the activity of MoTor. Lipidomics and transcriptomics analyses further confirmed that MoVast1 is an important regulator of lipid metabolism and the autophagy pathway. Our results revealed and characterized a novel sterol transfer protein important for <i>M. oryzae</i> pathogenicity.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Zhu</LastName><ForeName>Xue-Ming</ForeName><Initials>XM</Initials><AffiliationInfo><Affiliation>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>State Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences , Hangzhou 310021, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Lin</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cai</LastName><ForeName>Ying-Ying</ForeName><Initials>YY</Initials><AffiliationInfo><Affiliation>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wu</LastName><ForeName>Xi-Yu</ForeName><Initials>XY</Initials><AffiliationInfo><Affiliation>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shi</LastName><ForeName>Huan-Bin</ForeName><Initials>HB</Initials><AffiliationInfo><Affiliation>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liang</LastName><ForeName>Shuang</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Qu</LastName><ForeName>Ying-Min</ForeName><Initials>YM</Initials><AffiliationInfo><Affiliation>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Naqvi</LastName><ForeName>Naweed I</ForeName><Initials>NI</Initials><AffiliationInfo><Affiliation>Temasek Life Sciences Laboratory, Department of Biological Sciences, National University of Singapore , Singapore 117604.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Del Poeta</LastName><ForeName>Maurizio</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Department of Microbiology and Immunology, Stony Brook University , Stony Brook, New York, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Division of Infectious Diseases, Stony Brook University , Stony Brook, New York, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Veterans Affairs Medical Center , Northport, New York, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dong</LastName><ForeName>Bo</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Markey Cancer Center, University of Kentucky, College of Medicine , Lexington, KY 40506, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lin</LastName><ForeName>Fu-Cheng</ForeName><Initials>FC</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-4127-8143</Identifier><AffiliationInfo><Affiliation>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>State Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences , Hangzhou 310021, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Xiao-Hong</ForeName><Initials>XH</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-7466-1261</Identifier><AffiliationInfo><Affiliation>St ate Key Laboratory for Managing Biotic and Chemical Treats to the Quality and Safety of Agro-products, Institute of Biotechnology, Zhejiang University , Hangzhou 310058, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>11</Month><Day>11</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Autophagy</MedlineTA><NlmUniqueID>101265188</NlmUniqueID><ISSNLinking>1554-8627</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">MoTor</Keyword><Keyword MajorTopicYN="N">VASt-domain protein</Keyword><Keyword MajorTopicYN="N">autophagy</Keyword><Keyword MajorTopicYN="N">membrane tension</Keyword><Keyword MajorTopicYN="N">rice blast fungus</Keyword><Keyword MajorTopicYN="N">sterol homeostasis</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>11</Month><Day>12</Day><Hour>5</Hour><Minute>29</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>11</Month><Day>13</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>11</Month><Day>13</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">33176558</ArticleId><ArticleId IdType="doi">10.1080/15548627.2020.1848129</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>République populaire de Chine</li><li>États-Unis</li></country><region><li>Kentucky</li><li>Zhejiang</li><li>État de New York</li></region><settlement><li>Hangzhou</li></settlement></list><tree><noCountry><name sortKey="Naqvi, Naweed I" sort="Naqvi, Naweed I" uniqKey="Naqvi N" first="Naweed I" last="Naqvi">Naweed I. Naqvi</name></noCountry><country name="République populaire de Chine"><region name="Zhejiang"><name sortKey="Zhu, Xue Ming" sort="Zhu, Xue Ming" uniqKey="Zhu X" first="Xue-Ming" last="Zhu">Xue-Ming Zhu</name></region><name sortKey="Cai, Ying Ying" sort="Cai, Ying Ying" uniqKey="Cai Y" first="Ying-Ying" last="Cai">Ying-Ying Cai</name><name sortKey="Li, Lin" sort="Li, Lin" uniqKey="Li L" first="Lin" last="Li">Lin Li</name><name sortKey="Liang, Shuang" sort="Liang, Shuang" uniqKey="Liang S" first="Shuang" last="Liang">Shuang Liang</name><name sortKey="Lin, Fu Cheng" sort="Lin, Fu Cheng" uniqKey="Lin F" first="Fu-Cheng" last="Lin">Fu-Cheng Lin</name><name sortKey="Lin, Fu Cheng" sort="Lin, Fu Cheng" uniqKey="Lin F" first="Fu-Cheng" last="Lin">Fu-Cheng Lin</name><name sortKey="Liu, Xiao Hong" sort="Liu, Xiao Hong" uniqKey="Liu X" first="Xiao-Hong" last="Liu">Xiao-Hong Liu</name><name sortKey="Qu, Ying Min" sort="Qu, Ying Min" uniqKey="Qu Y" first="Ying-Min" last="Qu">Ying-Min Qu</name><name sortKey="Shi, Huan Bin" sort="Shi, Huan Bin" uniqKey="Shi H" first="Huan-Bin" last="Shi">Huan-Bin Shi</name><name sortKey="Wu, Xi Yu" sort="Wu, Xi Yu" uniqKey="Wu X" first="Xi-Yu" last="Wu">Xi-Yu Wu</name><name sortKey="Zhu, Xue Ming" sort="Zhu, Xue Ming" uniqKey="Zhu X" first="Xue-Ming" last="Zhu">Xue-Ming Zhu</name></country><country name="États-Unis"><region name="État de New York"><name sortKey="Del Poeta, Maurizio" sort="Del Poeta, Maurizio" uniqKey="Del Poeta M" first="Maurizio" last="Del Poeta">Maurizio Del Poeta</name></region><name sortKey="Del Poeta, Maurizio" sort="Del Poeta, Maurizio" uniqKey="Del Poeta M" first="Maurizio" last="Del Poeta">Maurizio Del Poeta</name><name sortKey="Del Poeta, Maurizio" sort="Del Poeta, Maurizio" uniqKey="Del Poeta M" first="Maurizio" last="Del Poeta">Maurizio Del Poeta</name><name sortKey="Dong, Bo" sort="Dong, Bo" uniqKey="Dong B" first="Bo" last="Dong">Bo Dong</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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