Phytophthora sojae Effector PsAvh240 Inhibits Host Aspartic Protease Secretion to Promote Infection.
Identifieur interne : 000556 ( Main/Corpus ); précédent : 000555; suivant : 000557Phytophthora sojae Effector PsAvh240 Inhibits Host Aspartic Protease Secretion to Promote Infection.
Auteurs : Baodian Guo ; Haonan Wang ; Bo Yang ; Wenjing Jiang ; Maofeng Jing ; Haiyang Li ; Yeqiang Xia ; Yuanpeng Xu ; Qinli Hu ; Fangfang Wang ; Feng Yu ; Yan Wang ; Wenwu Ye ; Suomeng Dong ; Weiman Xing ; Yuanchao WangSource :
- Molecular plant [ 1752-9867 ] ; 2019.
English descriptors
- KwdEn :
- Amino Acid Sequence (MeSH), Aspartic Acid Proteases (metabolism), Cell Membrane (metabolism), Host-Pathogen Interactions (MeSH), Models, Molecular (MeSH), Phytophthora (metabolism), Phytophthora (physiology), Plant Diseases (immunology), Plant Diseases (microbiology), Plant Immunity (MeSH), Protein Multimerization (MeSH), Protein Structure, Quaternary (MeSH), Protein Transport (MeSH), Soybeans (cytology), Soybeans (enzymology), Soybeans (immunology), Soybeans (microbiology), Virulence Factors (chemistry), Virulence Factors (metabolism).
- MESH :
- chemical , chemistry : Virulence Factors.
- chemical , metabolism : Aspartic Acid Proteases, Virulence Factors.
- cytology : Soybeans.
- enzymology : Soybeans.
- immunology : Plant Diseases, Soybeans.
- metabolism : Cell Membrane, Phytophthora.
- microbiology : Plant Diseases, Soybeans.
- physiology : Phytophthora.
- Amino Acid Sequence, Host-Pathogen Interactions, Models, Molecular, Plant Immunity, Protein Multimerization, Protein Structure, Quaternary, Protein Transport.
Abstract
Plants secrete defense molecules into the extracellular space (the apoplast) to combat attacking microbes. However, the mechanisms by which successful pathogens subvert plant apoplastic immunity remain poorly understood. In this study, we show that PsAvh240, a membrane-localized effector of the soybean pathogen Phytophthora sojae, promotes P. sojae infection in soybean hairy roots. We found that PsAvh240 interacts with the soybean-resistant aspartic protease GmAP1 in planta and suppresses the secretion of GmAP1 into the apoplast. By solving its crystal structure we revealed that PsAvh240 contain six α helices and two WY motifs. The first two α helices of PsAvh240 are responsible for its plasma membrane-localization and are required for PsAvh240's interaction with GmAP1. The second WY motifs of two PsAvh240 molecules form a handshake arrangement resulting in a handshake-like dimer. This dimerization is required for the effector's repression of GmAP1 secretion. Taken together, these data reveal that PsAvh240 localizes at the plasma membrane to interfere with GmAP1 secretion, which represents an effective mechanism by which effector proteins suppress plant apoplastic immunity.
DOI: 10.1016/j.molp.2019.01.017
PubMed: 30703565
Links to Exploration step
pubmed:30703565Le document en format XML
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<author><name sortKey="Wang, Haonan" sort="Wang, Haonan" uniqKey="Wang H" first="Haonan" last="Wang">Haonan Wang</name>
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<author><name sortKey="Yang, Bo" sort="Yang, Bo" uniqKey="Yang B" first="Bo" last="Yang">Bo Yang</name>
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<author><name sortKey="Li, Haiyang" sort="Li, Haiyang" uniqKey="Li H" first="Haiyang" last="Li">Haiyang Li</name>
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<author><name sortKey="Xia, Yeqiang" sort="Xia, Yeqiang" uniqKey="Xia Y" first="Yeqiang" last="Xia">Yeqiang Xia</name>
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<author><name sortKey="Xu, Yuanpeng" sort="Xu, Yuanpeng" uniqKey="Xu Y" first="Yuanpeng" last="Xu">Yuanpeng Xu</name>
<affiliation><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</nlm:affiliation>
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<author><name sortKey="Hu, Qinli" sort="Hu, Qinli" uniqKey="Hu Q" first="Qinli" last="Hu">Qinli Hu</name>
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<author><name sortKey="Wang, Fangfang" sort="Wang, Fangfang" uniqKey="Wang F" first="Fangfang" last="Wang">Fangfang Wang</name>
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<author><name sortKey="Yu, Feng" sort="Yu, Feng" uniqKey="Yu F" first="Feng" last="Yu">Feng Yu</name>
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<author><name sortKey="Wang, Yan" sort="Wang, Yan" uniqKey="Wang Y" first="Yan" last="Wang">Yan Wang</name>
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</affiliation>
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<author><name sortKey="Ye, Wenwu" sort="Ye, Wenwu" uniqKey="Ye W" first="Wenwu" last="Ye">Wenwu Ye</name>
<affiliation><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</nlm:affiliation>
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<author><name sortKey="Dong, Suomeng" sort="Dong, Suomeng" uniqKey="Dong S" first="Suomeng" last="Dong">Suomeng Dong</name>
<affiliation><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</nlm:affiliation>
</affiliation>
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<author><name sortKey="Xing, Weiman" sort="Xing, Weiman" uniqKey="Xing W" first="Weiman" last="Xing">Weiman Xing</name>
<affiliation><nlm:affiliation>National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 201204, China. Electronic address: wmxing@sibs.ac.cn.</nlm:affiliation>
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<author><name sortKey="Wang, Yuanchao" sort="Wang, Yuanchao" uniqKey="Wang Y" first="Yuanchao" last="Wang">Yuanchao Wang</name>
<affiliation><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China. Electronic address: wangyc@njau.edu.cn.</nlm:affiliation>
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<sourceDesc><biblStruct><analytic><title xml:lang="en">Phytophthora sojae Effector PsAvh240 Inhibits Host Aspartic Protease Secretion to Promote Infection.</title>
<author><name sortKey="Guo, Baodian" sort="Guo, Baodian" uniqKey="Guo B" first="Baodian" last="Guo">Baodian Guo</name>
<affiliation><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Wang, Haonan" sort="Wang, Haonan" uniqKey="Wang H" first="Haonan" last="Wang">Haonan Wang</name>
<affiliation><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Yang, Bo" sort="Yang, Bo" uniqKey="Yang B" first="Bo" last="Yang">Bo Yang</name>
<affiliation><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Jiang, Wenjing" sort="Jiang, Wenjing" uniqKey="Jiang W" first="Wenjing" last="Jiang">Wenjing Jiang</name>
<affiliation><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Jing, Maofeng" sort="Jing, Maofeng" uniqKey="Jing M" first="Maofeng" last="Jing">Maofeng Jing</name>
<affiliation><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</nlm:affiliation>
</affiliation>
</author>
<author><name sortKey="Li, Haiyang" sort="Li, Haiyang" uniqKey="Li H" first="Haiyang" last="Li">Haiyang Li</name>
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</affiliation>
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<author><name sortKey="Xia, Yeqiang" sort="Xia, Yeqiang" uniqKey="Xia Y" first="Yeqiang" last="Xia">Yeqiang Xia</name>
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</affiliation>
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<author><name sortKey="Xu, Yuanpeng" sort="Xu, Yuanpeng" uniqKey="Xu Y" first="Yuanpeng" last="Xu">Yuanpeng Xu</name>
<affiliation><nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</nlm:affiliation>
</affiliation>
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<author><name sortKey="Hu, Qinli" sort="Hu, Qinli" uniqKey="Hu Q" first="Qinli" last="Hu">Qinli Hu</name>
<affiliation><nlm:affiliation>National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 201204, China.</nlm:affiliation>
</affiliation>
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<author><name sortKey="Wang, Fangfang" sort="Wang, Fangfang" uniqKey="Wang F" first="Fangfang" last="Wang">Fangfang Wang</name>
<affiliation><nlm:affiliation>National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 201204, China.</nlm:affiliation>
</affiliation>
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<author><name sortKey="Yu, Feng" sort="Yu, Feng" uniqKey="Yu F" first="Feng" last="Yu">Feng Yu</name>
<affiliation><nlm:affiliation>Shanghai Institute of Applied Physics, Chinese Academy of Sciences, No. 239 Zhangheng Road, Shanghai 201204, China.</nlm:affiliation>
</affiliation>
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<author><name sortKey="Wang, Yan" sort="Wang, Yan" uniqKey="Wang Y" first="Yan" last="Wang">Yan Wang</name>
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</affiliation>
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<author><name sortKey="Ye, Wenwu" sort="Ye, Wenwu" uniqKey="Ye W" first="Wenwu" last="Ye">Wenwu Ye</name>
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</affiliation>
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<author><name sortKey="Dong, Suomeng" sort="Dong, Suomeng" uniqKey="Dong S" first="Suomeng" last="Dong">Suomeng Dong</name>
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</affiliation>
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<author><name sortKey="Xing, Weiman" sort="Xing, Weiman" uniqKey="Xing W" first="Weiman" last="Xing">Weiman Xing</name>
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<author><name sortKey="Wang, Yuanchao" sort="Wang, Yuanchao" uniqKey="Wang Y" first="Yuanchao" last="Wang">Yuanchao Wang</name>
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<imprint><date when="2019" type="published">2019</date>
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<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Amino Acid Sequence (MeSH)</term>
<term>Aspartic Acid Proteases (metabolism)</term>
<term>Cell Membrane (metabolism)</term>
<term>Host-Pathogen Interactions (MeSH)</term>
<term>Models, Molecular (MeSH)</term>
<term>Phytophthora (metabolism)</term>
<term>Phytophthora (physiology)</term>
<term>Plant Diseases (immunology)</term>
<term>Plant Diseases (microbiology)</term>
<term>Plant Immunity (MeSH)</term>
<term>Protein Multimerization (MeSH)</term>
<term>Protein Structure, Quaternary (MeSH)</term>
<term>Protein Transport (MeSH)</term>
<term>Soybeans (cytology)</term>
<term>Soybeans (enzymology)</term>
<term>Soybeans (immunology)</term>
<term>Soybeans (microbiology)</term>
<term>Virulence Factors (chemistry)</term>
<term>Virulence Factors (metabolism)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Virulence Factors</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Aspartic Acid Proteases</term>
<term>Virulence Factors</term>
</keywords>
<keywords scheme="MESH" qualifier="cytology" xml:lang="en"><term>Soybeans</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymology" xml:lang="en"><term>Soybeans</term>
</keywords>
<keywords scheme="MESH" qualifier="immunology" xml:lang="en"><term>Plant Diseases</term>
<term>Soybeans</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Cell Membrane</term>
<term>Phytophthora</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Plant Diseases</term>
<term>Soybeans</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Phytophthora</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Amino Acid Sequence</term>
<term>Host-Pathogen Interactions</term>
<term>Models, Molecular</term>
<term>Plant Immunity</term>
<term>Protein Multimerization</term>
<term>Protein Structure, Quaternary</term>
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<front><div type="abstract" xml:lang="en">Plants secrete defense molecules into the extracellular space (the apoplast) to combat attacking microbes. However, the mechanisms by which successful pathogens subvert plant apoplastic immunity remain poorly understood. In this study, we show that PsAvh240, a membrane-localized effector of the soybean pathogen Phytophthora sojae, promotes P. sojae infection in soybean hairy roots. We found that PsAvh240 interacts with the soybean-resistant aspartic protease GmAP1 in planta and suppresses the secretion of GmAP1 into the apoplast. By solving its crystal structure we revealed that PsAvh240 contain six α helices and two WY motifs. The first two α helices of PsAvh240 are responsible for its plasma membrane-localization and are required for PsAvh240's interaction with GmAP1. The second WY motifs of two PsAvh240 molecules form a handshake arrangement resulting in a handshake-like dimer. This dimerization is required for the effector's repression of GmAP1 secretion. Taken together, these data reveal that PsAvh240 localizes at the plasma membrane to interfere with GmAP1 secretion, which represents an effective mechanism by which effector proteins suppress plant apoplastic immunity.</div>
</front>
</TEI>
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<DateCompleted><Year>2019</Year>
<Month>11</Month>
<Day>22</Day>
</DateCompleted>
<DateRevised><Year>2019</Year>
<Month>11</Month>
<Day>22</Day>
</DateRevised>
<Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1752-9867</ISSN>
<JournalIssue CitedMedium="Internet"><Volume>12</Volume>
<Issue>4</Issue>
<PubDate><Year>2019</Year>
<Month>04</Month>
<Day>01</Day>
</PubDate>
</JournalIssue>
<Title>Molecular plant</Title>
<ISOAbbreviation>Mol Plant</ISOAbbreviation>
</Journal>
<ArticleTitle>Phytophthora sojae Effector PsAvh240 Inhibits Host Aspartic Protease Secretion to Promote Infection.</ArticleTitle>
<Pagination><MedlinePgn>552-564</MedlinePgn>
</Pagination>
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<Abstract><AbstractText>Plants secrete defense molecules into the extracellular space (the apoplast) to combat attacking microbes. However, the mechanisms by which successful pathogens subvert plant apoplastic immunity remain poorly understood. In this study, we show that PsAvh240, a membrane-localized effector of the soybean pathogen Phytophthora sojae, promotes P. sojae infection in soybean hairy roots. We found that PsAvh240 interacts with the soybean-resistant aspartic protease GmAP1 in planta and suppresses the secretion of GmAP1 into the apoplast. By solving its crystal structure we revealed that PsAvh240 contain six α helices and two WY motifs. The first two α helices of PsAvh240 are responsible for its plasma membrane-localization and are required for PsAvh240's interaction with GmAP1. The second WY motifs of two PsAvh240 molecules form a handshake arrangement resulting in a handshake-like dimer. This dimerization is required for the effector's repression of GmAP1 secretion. Taken together, these data reveal that PsAvh240 localizes at the plasma membrane to interfere with GmAP1 secretion, which represents an effective mechanism by which effector proteins suppress plant apoplastic immunity.</AbstractText>
<CopyrightInformation>Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Guo</LastName>
<ForeName>Baodian</ForeName>
<Initials>B</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Wang</LastName>
<ForeName>Haonan</ForeName>
<Initials>H</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Yang</LastName>
<ForeName>Bo</ForeName>
<Initials>B</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Jiang</LastName>
<ForeName>Wenjing</ForeName>
<Initials>W</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Jing</LastName>
<ForeName>Maofeng</ForeName>
<Initials>M</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Li</LastName>
<ForeName>Haiyang</ForeName>
<Initials>H</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Xia</LastName>
<ForeName>Yeqiang</ForeName>
<Initials>Y</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Xu</LastName>
<ForeName>Yuanpeng</ForeName>
<Initials>Y</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Hu</LastName>
<ForeName>Qinli</ForeName>
<Initials>Q</Initials>
<AffiliationInfo><Affiliation>National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 201204, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Wang</LastName>
<ForeName>Fangfang</ForeName>
<Initials>F</Initials>
<AffiliationInfo><Affiliation>National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 201204, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Yu</LastName>
<ForeName>Feng</ForeName>
<Initials>F</Initials>
<AffiliationInfo><Affiliation>Shanghai Institute of Applied Physics, Chinese Academy of Sciences, No. 239 Zhangheng Road, Shanghai 201204, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Wang</LastName>
<ForeName>Yan</ForeName>
<Initials>Y</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Ye</LastName>
<ForeName>Wenwu</ForeName>
<Initials>W</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Dong</LastName>
<ForeName>Suomeng</ForeName>
<Initials>S</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Xing</LastName>
<ForeName>Weiman</ForeName>
<Initials>W</Initials>
<AffiliationInfo><Affiliation>National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 201204, China. Electronic address: wmxing@sibs.ac.cn.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Wang</LastName>
<ForeName>Yuanchao</ForeName>
<Initials>Y</Initials>
<AffiliationInfo><Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China; Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), Nanjing 210095, China. Electronic address: wangyc@njau.edu.cn.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic"><Year>2019</Year>
<Month>01</Month>
<Day>28</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo><Country>England</Country>
<MedlineTA>Mol Plant</MedlineTA>
<NlmUniqueID>101465514</NlmUniqueID>
<ISSNLinking>1674-2052</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList><Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D037521">Virulence Factors</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>EC 3.4.-</RegistryNumber>
<NameOfSubstance UI="D057055">Aspartic Acid Proteases</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList><MeshHeading><DescriptorName UI="D000595" MajorTopicYN="N">Amino Acid Sequence</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D057055" MajorTopicYN="N">Aspartic Acid Proteases</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D002462" MajorTopicYN="N">Cell Membrane</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D054884" MajorTopicYN="Y">Host-Pathogen Interactions</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D008958" MajorTopicYN="N">Models, Molecular</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010838" MajorTopicYN="N">Phytophthora</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName>
<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D057865" MajorTopicYN="N">Plant Immunity</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D055503" MajorTopicYN="N">Protein Multimerization</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D020836" MajorTopicYN="N">Protein Structure, Quaternary</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D021381" MajorTopicYN="N">Protein Transport</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D013025" MajorTopicYN="N">Soybeans</DescriptorName>
<QualifierName UI="Q000166" MajorTopicYN="N">cytology</QualifierName>
<QualifierName UI="Q000201" MajorTopicYN="Y">enzymology</QualifierName>
<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D037521" MajorTopicYN="N">Virulence Factors</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Phytophthora sojae effector</Keyword>
<Keyword MajorTopicYN="Y">effector triggered susceptibility</Keyword>
<Keyword MajorTopicYN="Y">handshake-like dimer</Keyword>
<Keyword MajorTopicYN="Y">plant apoplastic immunity</Keyword>
<Keyword MajorTopicYN="Y">soybean aspartic protease</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year>
<Month>10</Month>
<Day>10</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="revised"><Year>2018</Year>
<Month>12</Month>
<Day>20</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted"><Year>2019</Year>
<Month>01</Month>
<Day>18</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed"><Year>2019</Year>
<Month>2</Month>
<Day>1</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline"><Year>2019</Year>
<Month>11</Month>
<Day>23</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez"><Year>2019</Year>
<Month>2</Month>
<Day>1</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList><ArticleId IdType="pubmed">30703565</ArticleId>
<ArticleId IdType="pii">S1674-2052(19)30023-1</ArticleId>
<ArticleId IdType="doi">10.1016/j.molp.2019.01.017</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
</record>
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