Serveur d'exploration sur les effecteurs de phytopathogènes

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N-glycosylation shields Phytophthora sojae apoplastic effector PsXEG1 from a specific host aspartic protease.

Identifieur interne : 000101 ( Main/Exploration ); précédent : 000100; suivant : 000102

N-glycosylation shields Phytophthora sojae apoplastic effector PsXEG1 from a specific host aspartic protease.

Auteurs : Yeqiang Xia [République populaire de Chine] ; Zhenchuan Ma [République populaire de Chine] ; Min Qiu [République populaire de Chine] ; Baodian Guo [République populaire de Chine] ; Qi Zhang [République populaire de Chine] ; Haibin Jiang [République populaire de Chine] ; Baiyu Zhang [République populaire de Chine] ; Yachun Lin [République populaire de Chine] ; Mingrun Xuan [République populaire de Chine] ; Liang Sun [République populaire de Chine] ; Haidong Shu [République populaire de Chine] ; Junhua Xiao [République populaire de Chine] ; Wenwu Ye [République populaire de Chine] ; Yan Wang [République populaire de Chine] ; Yiming Wang [République populaire de Chine] ; Suomeng Dong [République populaire de Chine] ; Brett M. Tyler [États-Unis] ; Yuanchao Wang [République populaire de Chine]

Source :

RBID : pubmed:33082226

Abstract

Hosts and pathogens are engaged in a continuous evolutionary struggle for physiological dominance. A major site of this struggle is the apoplast. In Phytophthora sojae-soybean interactions, PsXEG1, a pathogen-secreted apoplastic endoglucanase, is a key focal point of this struggle, and the subject of two layers of host defense and pathogen counterdefense. Here, we show that N-glycosylation of PsXEG1 represents an additional layer of this coevolutionary struggle, protecting PsXEG1 against a host apoplastic aspartic protease, GmAP5, that specifically targets PsXEG1. This posttranslational modification also attenuated binding by the previously described host inhibitor, GmGIP1. N-glycosylation of PsXEG1 at N174 and N190 inhibited binding and degradation by GmAP5 and was essential for PsXEG1's full virulence contribution, except in GmAP5-silenced soybeans. Silencing of GmAP5 reduced soybean resistance against WT P. sojae but not against PsXEG1 deletion strains of P. sojae. The crucial role of N-glycosylation within the three layers of defense and counterdefense centered on PsXEG1 highlight the critical importance of this conserved apoplastic effector and its posttranslational modification in Phytophthora-host coevolutionary conflict.

DOI: 10.1073/pnas.2012149117
PubMed: 33082226


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<name sortKey="Sun, Liang" sort="Sun, Liang" uniqKey="Sun L" first="Liang" last="Sun">Liang Sun</name>
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<name sortKey="Shu, Haidong" sort="Shu, Haidong" uniqKey="Shu H" first="Haidong" last="Shu">Haidong Shu</name>
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<name sortKey="Xiao, Junhua" sort="Xiao, Junhua" uniqKey="Xiao J" first="Junhua" last="Xiao">Junhua Xiao</name>
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<name sortKey="Wang, Yiming" sort="Wang, Yiming" uniqKey="Wang Y" first="Yiming" last="Wang">Yiming Wang</name>
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<nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</nlm:affiliation>
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<nlm:affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
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<wicri:noRegion>Nanjing 210095</wicri:noRegion>
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<nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing</wicri:regionArea>
<wicri:noRegion>210095 Nanjing</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Wang, Yiming" sort="Wang, Yiming" uniqKey="Wang Y" first="Yiming" last="Wang">Yiming Wang</name>
<affiliation wicri:level="1">
<nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing</wicri:regionArea>
<wicri:noRegion>210095 Nanjing</wicri:noRegion>
</affiliation>
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<country xml:lang="fr">République populaire de Chine</country>
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<wicri:noRegion>Nanjing 210095</wicri:noRegion>
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<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing</wicri:regionArea>
<wicri:noRegion>210095 Nanjing</wicri:noRegion>
</affiliation>
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<author>
<name sortKey="Dong, Suomeng" sort="Dong, Suomeng" uniqKey="Dong S" first="Suomeng" last="Dong">Suomeng Dong</name>
<affiliation wicri:level="1">
<nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing</wicri:regionArea>
<wicri:noRegion>210095 Nanjing</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1">
<nlm:affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Nanjing 210095</wicri:regionArea>
<wicri:noRegion>Nanjing 210095</wicri:noRegion>
</affiliation>
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<nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China.</nlm:affiliation>
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<wicri:regionArea>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing</wicri:regionArea>
<wicri:noRegion>210095 Nanjing</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Tyler, Brett M" sort="Tyler, Brett M" uniqKey="Tyler B" first="Brett M" last="Tyler">Brett M. Tyler</name>
<affiliation wicri:level="2">
<nlm:affiliation>Center for Genome Research and Biocomputing, Oregon State University, Corvallis, OR 97331.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Oregon</region>
</placeName>
<wicri:cityArea>Center for Genome Research and Biocomputing, Oregon State University, Corvallis</wicri:cityArea>
</affiliation>
<affiliation wicri:level="2">
<nlm:affiliation>Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Oregon</region>
</placeName>
<wicri:cityArea>Department of Botany and Plant Pathology, Oregon State University, Corvallis</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Wang, Yuanchao" sort="Wang, Yuanchao" uniqKey="Wang Y" first="Yuanchao" last="Wang">Yuanchao Wang</name>
<affiliation wicri:level="1">
<nlm:affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China; wangyc@njau.edu.cn.</nlm:affiliation>
<country wicri:rule="url">République populaire de Chine</country>
<wicri:regionArea>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing</wicri:regionArea>
<wicri:noRegion>210095 Nanjing</wicri:noRegion>
</affiliation>
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<nlm:affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
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<wicri:noRegion>Nanjing 210095</wicri:noRegion>
</affiliation>
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<nlm:affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China.</nlm:affiliation>
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</affiliation>
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<series>
<title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
<idno type="eISSN">1091-6490</idno>
<imprint>
<date when="2020" type="published">2020</date>
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<div type="abstract" xml:lang="en">Hosts and pathogens are engaged in a continuous evolutionary struggle for physiological dominance. A major site of this struggle is the apoplast. In
<i>Phytophthora sojae</i>
-soybean interactions, PsXEG1, a pathogen-secreted apoplastic endoglucanase, is a key focal point of this struggle, and the subject of two layers of host defense and pathogen counterdefense. Here, we show that N-glycosylation of PsXEG1 represents an additional layer of this coevolutionary struggle, protecting PsXEG1 against a host apoplastic aspartic protease, GmAP5, that specifically targets PsXEG1. This posttranslational modification also attenuated binding by the previously described host inhibitor, GmGIP1. N-glycosylation of PsXEG1 at N174 and N190 inhibited binding and degradation by GmAP5 and was essential for
<i>PsXEG1</i>
's full virulence contribution, except in GmAP5-silenced soybeans. Silencing of GmAP5 reduced soybean resistance against WT
<i>P. sojae</i>
but not against
<i>PsXEG1</i>
deletion strains of
<i>P. sojae.</i>
The crucial role of N-glycosylation within the three layers of defense and counterdefense centered on PsXEG1 highlight the critical importance of this conserved apoplastic effector and its posttranslational modification in
<i>Phytophthora</i>
-host coevolutionary conflict.</div>
</front>
</TEI>
<pubmed>
<MedlineCitation Status="In-Data-Review" Owner="NLM">
<PMID Version="1">33082226</PMID>
<DateRevised>
<Year>2020</Year>
<Month>11</Month>
<Day>04</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1091-6490</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>117</Volume>
<Issue>44</Issue>
<PubDate>
<Year>2020</Year>
<Month>Nov</Month>
<Day>03</Day>
</PubDate>
</JournalIssue>
<Title>Proceedings of the National Academy of Sciences of the United States of America</Title>
<ISOAbbreviation>Proc Natl Acad Sci U S A</ISOAbbreviation>
</Journal>
<ArticleTitle>N
<i>-</i>
glycosylation shields
<i>Phytophthora sojae</i>
apoplastic effector PsXEG1 from a specific host aspartic protease.</ArticleTitle>
<Pagination>
<MedlinePgn>27685-27693</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1073/pnas.2012149117</ELocationID>
<Abstract>
<AbstractText>Hosts and pathogens are engaged in a continuous evolutionary struggle for physiological dominance. A major site of this struggle is the apoplast. In
<i>Phytophthora sojae</i>
-soybean interactions, PsXEG1, a pathogen-secreted apoplastic endoglucanase, is a key focal point of this struggle, and the subject of two layers of host defense and pathogen counterdefense. Here, we show that N-glycosylation of PsXEG1 represents an additional layer of this coevolutionary struggle, protecting PsXEG1 against a host apoplastic aspartic protease, GmAP5, that specifically targets PsXEG1. This posttranslational modification also attenuated binding by the previously described host inhibitor, GmGIP1. N-glycosylation of PsXEG1 at N174 and N190 inhibited binding and degradation by GmAP5 and was essential for
<i>PsXEG1</i>
's full virulence contribution, except in GmAP5-silenced soybeans. Silencing of GmAP5 reduced soybean resistance against WT
<i>P. sojae</i>
but not against
<i>PsXEG1</i>
deletion strains of
<i>P. sojae.</i>
The crucial role of N-glycosylation within the three layers of defense and counterdefense centered on PsXEG1 highlight the critical importance of this conserved apoplastic effector and its posttranslational modification in
<i>Phytophthora</i>
-host coevolutionary conflict.</AbstractText>
<CopyrightInformation>Copyright © 2020 the Author(s). Published by PNAS.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Xia</LastName>
<ForeName>Yeqiang</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Ma</LastName>
<ForeName>Zhenchuan</ForeName>
<Initials>Z</Initials>
<Identifier Source="ORCID">https://orcid.org/0000-0002-8478-2833</Identifier>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
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<Affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Qiu</LastName>
<ForeName>Min</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
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</Author>
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<LastName>Guo</LastName>
<ForeName>Baodian</ForeName>
<Initials>B</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
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<Affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
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<LastName>Zhang</LastName>
<ForeName>Qi</ForeName>
<Initials>Q</Initials>
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<Affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
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<Affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
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<Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
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</Author>
<Author ValidYN="Y">
<LastName>Jiang</LastName>
<ForeName>Haibin</ForeName>
<Initials>H</Initials>
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<Affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
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</Author>
<Author ValidYN="Y">
<LastName>Zhang</LastName>
<ForeName>Baiyu</ForeName>
<Initials>B</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
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<Affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
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<Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
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<LastName>Lin</LastName>
<ForeName>Yachun</ForeName>
<Initials>Y</Initials>
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<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
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<Affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
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<Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Xuan</LastName>
<ForeName>Mingrun</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
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<Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
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</Author>
<Author ValidYN="Y">
<LastName>Sun</LastName>
<ForeName>Liang</ForeName>
<Initials>L</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
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<Affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
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</Author>
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<LastName>Shu</LastName>
<ForeName>Haidong</ForeName>
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<Affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
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<Author ValidYN="Y">
<LastName>Xiao</LastName>
<ForeName>Junhua</ForeName>
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<Affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
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<LastName>Ye</LastName>
<ForeName>Wenwu</ForeName>
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<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
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<Affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
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<Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wang</LastName>
<ForeName>Yan</ForeName>
<Initials>Y</Initials>
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<Affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
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<Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wang</LastName>
<ForeName>Yiming</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Dong</LastName>
<ForeName>Suomeng</ForeName>
<Initials>S</Initials>
<Identifier Source="ORCID">https://orcid.org/0000-0002-9623-6776</Identifier>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Tyler</LastName>
<ForeName>Brett M</ForeName>
<Initials>BM</Initials>
<Identifier Source="ORCID">https://orcid.org/0000-0003-1549-2987</Identifier>
<AffiliationInfo>
<Affiliation>Center for Genome Research and Biocomputing, Oregon State University, Corvallis, OR 97331.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wang</LastName>
<ForeName>Yuanchao</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Nanjing Agricultural University, 210095 Nanjing, China; wangyc@njau.edu.cn.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Key Laboratory of Integrated Management of Crop Diseases and Pests (Ministry of Education), College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>The Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2020</Year>
<Month>10</Month>
<Day>20</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>United States</Country>
<MedlineTA>Proc Natl Acad Sci U S A</MedlineTA>
<NlmUniqueID>7505876</NlmUniqueID>
<ISSNLinking>0027-8424</ISSNLinking>
</MedlineJournalInfo>
<CitationSubset>IM</CitationSubset>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">N-glycosylation</Keyword>
<Keyword MajorTopicYN="N">P. sojae</Keyword>
<Keyword MajorTopicYN="N">apoplast</Keyword>
<Keyword MajorTopicYN="N">aspartic protease</Keyword>
<Keyword MajorTopicYN="N">immunity</Keyword>
</KeywordList>
<CoiStatement>The authors declare no competing interest.</CoiStatement>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="pubmed">
<Year>2020</Year>
<Month>10</Month>
<Day>22</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2020</Year>
<Month>10</Month>
<Day>22</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2020</Year>
<Month>10</Month>
<Day>21</Day>
<Hour>5</Hour>
<Minute>53</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">33082226</ArticleId>
<ArticleId IdType="pii">2012149117</ArticleId>
<ArticleId IdType="doi">10.1073/pnas.2012149117</ArticleId>
</ArticleIdList>
<ReferenceList>
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<li>États-Unis</li>
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<name sortKey="Wang, Yan" sort="Wang, Yan" uniqKey="Wang Y" first="Yan" last="Wang">Yan Wang</name>
<name sortKey="Wang, Yan" sort="Wang, Yan" uniqKey="Wang Y" first="Yan" last="Wang">Yan Wang</name>
<name sortKey="Wang, Yiming" sort="Wang, Yiming" uniqKey="Wang Y" first="Yiming" last="Wang">Yiming Wang</name>
<name sortKey="Wang, Yiming" sort="Wang, Yiming" uniqKey="Wang Y" first="Yiming" last="Wang">Yiming Wang</name>
<name sortKey="Wang, Yiming" sort="Wang, Yiming" uniqKey="Wang Y" first="Yiming" last="Wang">Yiming Wang</name>
<name sortKey="Wang, Yuanchao" sort="Wang, Yuanchao" uniqKey="Wang Y" first="Yuanchao" last="Wang">Yuanchao Wang</name>
<name sortKey="Wang, Yuanchao" sort="Wang, Yuanchao" uniqKey="Wang Y" first="Yuanchao" last="Wang">Yuanchao Wang</name>
<name sortKey="Wang, Yuanchao" sort="Wang, Yuanchao" uniqKey="Wang Y" first="Yuanchao" last="Wang">Yuanchao Wang</name>
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<name sortKey="Xiao, Junhua" sort="Xiao, Junhua" uniqKey="Xiao J" first="Junhua" last="Xiao">Junhua Xiao</name>
<name sortKey="Xiao, Junhua" sort="Xiao, Junhua" uniqKey="Xiao J" first="Junhua" last="Xiao">Junhua Xiao</name>
<name sortKey="Xiao, Junhua" sort="Xiao, Junhua" uniqKey="Xiao J" first="Junhua" last="Xiao">Junhua Xiao</name>
<name sortKey="Xuan, Mingrun" sort="Xuan, Mingrun" uniqKey="Xuan M" first="Mingrun" last="Xuan">Mingrun Xuan</name>
<name sortKey="Xuan, Mingrun" sort="Xuan, Mingrun" uniqKey="Xuan M" first="Mingrun" last="Xuan">Mingrun Xuan</name>
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<name sortKey="Ye, Wenwu" sort="Ye, Wenwu" uniqKey="Ye W" first="Wenwu" last="Ye">Wenwu Ye</name>
<name sortKey="Ye, Wenwu" sort="Ye, Wenwu" uniqKey="Ye W" first="Wenwu" last="Ye">Wenwu Ye</name>
<name sortKey="Ye, Wenwu" sort="Ye, Wenwu" uniqKey="Ye W" first="Wenwu" last="Ye">Wenwu Ye</name>
<name sortKey="Zhang, Baiyu" sort="Zhang, Baiyu" uniqKey="Zhang B" first="Baiyu" last="Zhang">Baiyu Zhang</name>
<name sortKey="Zhang, Baiyu" sort="Zhang, Baiyu" uniqKey="Zhang B" first="Baiyu" last="Zhang">Baiyu Zhang</name>
<name sortKey="Zhang, Baiyu" sort="Zhang, Baiyu" uniqKey="Zhang B" first="Baiyu" last="Zhang">Baiyu Zhang</name>
<name sortKey="Zhang, Qi" sort="Zhang, Qi" uniqKey="Zhang Q" first="Qi" last="Zhang">Qi Zhang</name>
<name sortKey="Zhang, Qi" sort="Zhang, Qi" uniqKey="Zhang Q" first="Qi" last="Zhang">Qi Zhang</name>
<name sortKey="Zhang, Qi" sort="Zhang, Qi" uniqKey="Zhang Q" first="Qi" last="Zhang">Qi Zhang</name>
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<name sortKey="Tyler, Brett M" sort="Tyler, Brett M" uniqKey="Tyler B" first="Brett M" last="Tyler">Brett M. Tyler</name>
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