Identification and Functional Analysis of AopN, an Acidovorax Citrulli Effector that Induces Programmed Cell Death in Plants.
Identifieur interne : 000138 ( Main/Exploration ); précédent : 000137; suivant : 000139Identification and Functional Analysis of AopN, an Acidovorax Citrulli Effector that Induces Programmed Cell Death in Plants.
Auteurs : Xiaoxiao Zhang [République populaire de Chine] ; Mei Zhao [États-Unis] ; Jie Jiang [République populaire de Chine] ; Linlin Yang [République populaire de Chine] ; Yuwen Yang [République populaire de Chine] ; Shanshan Yang [République populaire de Chine] ; Ron Walcott [États-Unis] ; Dewen Qiu [République populaire de Chine] ; Tingchang Zhao [République populaire de Chine]Source :
- International journal of molecular sciences [ 1422-0067 ] ; 2020.
Abstract
Bacterial fruit blotch (BFB), caused by Acidovorax citrulli, seriously affects watermelon and other cucurbit crops, resulting in significant economic losses. However, the pathogenicity mechanism of A. citrulli is not well understood. Plant pathogenic bacteria often suppress the plant immune response by secreting effector proteins. Thus, identifying A. citrulli effector proteins and determining their functions may improve our understanding of the underlying pathogenetic mechanisms. In this study, a novel effector, AopN, which is localized on the cell membrane of Nicotiana benthamiana, was identified. The functional analysis revealed that AopN significantly inhibited the flg22-induced reactive oxygen species burst. AopN induced a programmed cell death (PCD) response. Unlike its homologous protein, the ability of AopN to induce PCD was dependent on two motifs of unknown functions (including DUP4129 and Cpta_toxin), but was not dependent on LXXLL domain. More importantly, the virulence of the aopN mutant of A. citrulli in N. benthamiana significantly decreased, indicating that it was a core effector. Further analysis revealed that AopN interacted with watermelon ClHIPP and ClLTP, which responds to A. citrulli strain Aac5 infection at the transcription level. Collectively, these findings indicate that AopN suppresses plant immunity and activates the effector-triggered immunity pathway.
DOI: 10.3390/ijms21176050
PubMed: 32842656
PubMed Central: PMC7504669
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Zhang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Zhao, Mei" sort="Zhao, Mei" uniqKey="Zhao M" first="Mei" last="Zhao">Mei Zhao</name><affiliation wicri:level="2"><nlm:affiliation>Department of Plant Pathology, University of Georgia, Athens, GA 30602, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Pathology, University of Georgia, Athens, GA 30602</wicri:regionArea><placeName><region type="state">Géorgie (États-Unis)</region></placeName></affiliation></author><author><name sortKey="Jiang, Jie" sort="Jiang, Jie" uniqKey="Jiang J" first="Jie" last="Jiang">Jie Jiang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Yang, Linlin" sort="Yang, Linlin" uniqKey="Yang L" first="Linlin" last="Yang">Linlin Yang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Yang, Yuwen" sort="Yang, Yuwen" uniqKey="Yang Y" first="Yuwen" last="Yang">Yuwen Yang</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Yang, Shanshan" sort="Yang, Shanshan" uniqKey="Yang S" first="Shanshan" last="Yang">Shanshan Yang</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100193, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100193</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Walcott, Ron" sort="Walcott, Ron" uniqKey="Walcott R" first="Ron" last="Walcott">Ron Walcott</name><affiliation wicri:level="2"><nlm:affiliation>Department of Plant Pathology, University of Georgia, Athens, GA 30602, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Pathology, University of Georgia, Athens, GA 30602</wicri:regionArea><placeName><region type="state">Géorgie (États-Unis)</region></placeName></affiliation></author><author><name sortKey="Qiu, Dewen" sort="Qiu, Dewen" uniqKey="Qiu D" first="Dewen" last="Qiu">Dewen Qiu</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Zhao, Tingchang" sort="Zhao, Tingchang" uniqKey="Zhao T" first="Tingchang" last="Zhao">Tingchang Zhao</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author></analytic><series><title level="j">International journal of molecular sciences</title><idno type="eISSN">1422-0067</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">Bacterial fruit blotch (BFB), caused by <i>Acidovorax citrulli</i>, seriously affects watermelon and other cucurbit crops, resulting in significant economic losses. However, the pathogenicity mechanism of <i>A. citrulli</i> is not well understood. Plant pathogenic bacteria often suppress the plant immune response by secreting effector proteins. Thus, identifying <i>A. citrulli</i> effector proteins and determining their functions may improve our understanding of the underlying pathogenetic mechanisms. In this study, a novel effector, AopN, which is localized on the cell membrane of <i>Nicotiana benthamiana,</i> was identified. The functional analysis revealed that AopN significantly inhibited the flg22-induced reactive oxygen species burst. AopN induced a programmed cell death (PCD) response. Unlike its homologous protein, the ability of AopN to induce PCD was dependent on two motifs of unknown functions (including DUP4129 and Cpta_toxin), but was not dependent on LXXLL domain. More importantly, the virulence of the <i>aopN</i> mutant of <i>A. citrulli</i> in <i>N. benthamiana</i> significantly decreased, indicating that it was a core effector. Further analysis revealed that AopN interacted with watermelon ClHIPP and ClLTP, which responds to <i>A. citrulli</i> strain Aac5 infection at the transcription level. Collectively, these findings indicate that AopN suppresses plant immunity and activates the effector-triggered immunity pathway.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32842656</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>01</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">1422-0067</ISSN><JournalIssue CitedMedium="Internet"><Volume>21</Volume><Issue>17</Issue><PubDate><Year>2020</Year><Month>Aug</Month><Day>22</Day></PubDate></JournalIssue><Title>International journal of molecular sciences</Title><ISOAbbreviation>Int J Mol Sci</ISOAbbreviation></Journal><ArticleTitle>Identification and Functional Analysis of AopN, an <i>Acidovorax Citrulli</i> Effector that Induces Programmed Cell Death in Plants.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">E6050</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.3390/ijms21176050</ELocationID><Abstract><AbstractText>Bacterial fruit blotch (BFB), caused by <i>Acidovorax citrulli</i>, seriously affects watermelon and other cucurbit crops, resulting in significant economic losses. However, the pathogenicity mechanism of <i>A. citrulli</i> is not well understood. Plant pathogenic bacteria often suppress the plant immune response by secreting effector proteins. Thus, identifying <i>A. citrulli</i> effector proteins and determining their functions may improve our understanding of the underlying pathogenetic mechanisms. In this study, a novel effector, AopN, which is localized on the cell membrane of <i>Nicotiana benthamiana,</i> was identified. The functional analysis revealed that AopN significantly inhibited the flg22-induced reactive oxygen species burst. AopN induced a programmed cell death (PCD) response. Unlike its homologous protein, the ability of AopN to induce PCD was dependent on two motifs of unknown functions (including DUP4129 and Cpta_toxin), but was not dependent on LXXLL domain. More importantly, the virulence of the <i>aopN</i> mutant of <i>A. citrulli</i> in <i>N. benthamiana</i> significantly decreased, indicating that it was a core effector. Further analysis revealed that AopN interacted with watermelon ClHIPP and ClLTP, which responds to <i>A. citrulli</i> strain Aac5 infection at the transcription level. Collectively, these findings indicate that AopN suppresses plant immunity and activates the effector-triggered immunity pathway.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Xiaoxiao</ForeName><Initials>X</Initials><Identifier Source="ORCID">0000-0002-9442-3711</Identifier><AffiliationInfo><Affiliation>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhao</LastName><ForeName>Mei</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, University of Georgia, Athens, GA 30602, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jiang</LastName><ForeName>Jie</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yang</LastName><ForeName>Linlin</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yang</LastName><ForeName>Yuwen</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yang</LastName><ForeName>Shanshan</ForeName><Initials>S</Initials><Identifier Source="ORCID">0000-0002-2371-3981</Identifier><AffiliationInfo><Affiliation>Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100193, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Walcott</LastName><ForeName>Ron</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, University of Georgia, Athens, GA 30602, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Qiu</LastName><ForeName>Dewen</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhao</LastName><ForeName>Tingchang</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>6204046</GrantID><Agency>Beijing Natural Science Foundation of China</Agency><Country></Country></Grant><Grant><GrantID>2018YFD0201300</GrantID><Agency>National Key Research and Development Program of China</Agency><Country></Country></Grant><Grant><GrantID>2016YFD0201004</GrantID><Agency>National Key Research and Development Program of China</Agency><Country></Country></Grant><Grant><GrantID>CARS-25</GrantID><Agency>China earmarked Fund for Modern Agro-industry Technology Research System</Agency><Country></Country></Grant><Grant><GrantID>2017YFD0201608</GrantID><Agency>National Key Research and Development Program of China</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>08</Month><Day>22</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Int J Mol Sci</MedlineTA><NlmUniqueID>101092791</NlmUniqueID><ISSNLinking>1422-0067</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Acidovorax citrulli</Keyword><Keyword MajorTopicYN="N">AopN</Keyword><Keyword MajorTopicYN="N">effector-triggered immunity</Keyword><Keyword MajorTopicYN="N">plant pathogen</Keyword><Keyword MajorTopicYN="N">programmed cell death</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>07</Month><Day>08</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>08</Month><Day>01</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>08</Month><Day>18</Day></PubMedPubDate><PubMedPubDate 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last="Qiu">Dewen Qiu</name><name sortKey="Yang, Linlin" sort="Yang, Linlin" uniqKey="Yang L" first="Linlin" last="Yang">Linlin Yang</name><name sortKey="Yang, Shanshan" sort="Yang, Shanshan" uniqKey="Yang S" first="Shanshan" last="Yang">Shanshan Yang</name><name sortKey="Yang, Yuwen" sort="Yang, Yuwen" uniqKey="Yang Y" first="Yuwen" last="Yang">Yuwen Yang</name><name sortKey="Zhao, Tingchang" sort="Zhao, Tingchang" uniqKey="Zhao T" first="Tingchang" last="Zhao">Tingchang Zhao</name></country><country name="États-Unis"><region name="Géorgie (États-Unis)"><name sortKey="Zhao, Mei" sort="Zhao, Mei" uniqKey="Zhao M" first="Mei" last="Zhao">Mei Zhao</name></region><name sortKey="Walcott, Ron" sort="Walcott, Ron" uniqKey="Walcott R" first="Ron" last="Walcott">Ron Walcott</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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