The Arabidopsis thaliana gene AtERF019 negatively regulates plant resistance to Phytophthora parasitica by suppressing PAMP-triggered immunity.
Identifieur interne : 000034 ( Main/Exploration ); précédent : 000033; suivant : 000035The Arabidopsis thaliana gene AtERF019 negatively regulates plant resistance to Phytophthora parasitica by suppressing PAMP-triggered immunity.
Auteurs : Wenqin Lu [République populaire de Chine] ; Fengyan Deng [République populaire de Chine] ; Jinbu Jia [République populaire de Chine] ; Xiaokang Chen [République populaire de Chine] ; Jinfang Li [République populaire de Chine] ; Qujiang Wen [République populaire de Chine] ; Tingting Li [République populaire de Chine] ; Yuling Meng [République populaire de Chine] ; Weixing Shan [République populaire de Chine]Source :
- Molecular plant pathology [ 1364-3703 ] ; 2020.
Abstract
Phytophthora species are destructive plant pathogens that cause significant crop losses worldwide. To understand plant susceptibility to oomycete pathogens and to explore novel disease resistance strategies, we employed the Arabidopsis thaliana-Phytophthora parasitica model pathosystem and screened for A. thaliana T-DNA insertion mutant lines resistant to P. parasitica. This led to the identification of the resistant mutant 267-31, which carries two T-DNA insertion sites in the promoter region of the ethylene-responsive factor 19 gene (ERF019). Quantitative reverse transcription PCR (RT-qPCR) assays showed that the expression of ERF019 was induced during P. parasitica infection in the wild type, which was suppressed in the 267-31 mutant. Additional erf019 mutants were generated using CRISPR/Cas9 technology and were confirmed to have increased resistance to P. parasitica. In contrast, ERF019 overexpression lines were more susceptible. Transient overexpression assays in Nicotiana benthamiana showed that the nuclear localization of ERF019 is crucial for its susceptible function. RT-qPCR analyses showed that the expression of marker genes for multiple defence pathways was significantly up-regulated in the mutant compared with the wild type during infection. Flg22-induced hydrogen peroxide accumulation and reactive oxygen species burst were impaired in ERF019 overexpression lines, and flg22-induced MAPK activation was enhanced in erf019 mutants. Moreover, transient overexpression of ERF019 strongly suppressed INF-triggered cell death in N. benthamiana. These results reveal the importance of ERF019 in mediating plant susceptibility to P. parasitica through suppression of pathogen-associated molecular pattern-triggered immunity.
DOI: 10.1111/mpp.12971
PubMed: 32725756
PubMed Central: PMC7411552
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China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling</wicri:regionArea><wicri:noRegion>Yangling</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:32725756</idno><idno type="pmid">32725756</idno><idno type="doi">10.1111/mpp.12971</idno><idno type="pmc">PMC7411552</idno><idno type="wicri:Area/Main/Corpus">000118</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000118</idno><idno type="wicri:Area/Main/Curation">000118</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000118</idno><idno type="wicri:Area/Main/Exploration">000118</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">The Arabidopsis thaliana gene AtERF019 negatively regulates plant resistance to Phytophthora parasitica by suppressing PAMP-triggered immunity.</title><author><name sortKey="Lu, Wenqin" sort="Lu, Wenqin" uniqKey="Lu W" first="Wenqin" last="Lu">Wenqin Lu</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling</wicri:regionArea><wicri:noRegion>Yangling</wicri:noRegion></affiliation></author><author><name sortKey="Deng, Fengyan" sort="Deng, Fengyan" uniqKey="Deng F" first="Fengyan" last="Deng">Fengyan Deng</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Life Sciences, Northwest A&F University, Yangling, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Life Sciences, Northwest A&F University, Yangling</wicri:regionArea><wicri:noRegion>Yangling</wicri:noRegion></affiliation></author><author><name sortKey="Jia, Jinbu" sort="Jia, Jinbu" uniqKey="Jia J" first="Jinbu" last="Jia">Jinbu Jia</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling</wicri:regionArea><wicri:noRegion>Yangling</wicri:noRegion></affiliation><affiliation wicri:level="3"><nlm:affiliation>Institute of Plant and Food Science, Department of Biology, Southern University of Science and Technology, Shenzhen, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Institute of Plant and Food Science, Department of Biology, Southern University of Science and Technology, Shenzhen</wicri:regionArea><placeName><settlement type="city">Shenzhen</settlement><region type="province">Guangdong</region></placeName></affiliation></author><author><name sortKey="Chen, Xiaokang" sort="Chen, Xiaokang" uniqKey="Chen X" first="Xiaokang" last="Chen">Xiaokang Chen</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Horticulture, Northwest A&F University, Yangling, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Horticulture, Northwest A&F University, Yangling</wicri:regionArea><wicri:noRegion>Yangling</wicri:noRegion></affiliation></author><author><name sortKey="Li, Jinfang" sort="Li, Jinfang" uniqKey="Li J" first="Jinfang" last="Li">Jinfang Li</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling</wicri:regionArea><wicri:noRegion>Yangling</wicri:noRegion></affiliation></author><author><name sortKey="Wen, Qujiang" sort="Wen, Qujiang" uniqKey="Wen Q" first="Qujiang" last="Wen">Qujiang Wen</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling</wicri:regionArea><wicri:noRegion>Yangling</wicri:noRegion></affiliation></author><author><name sortKey="Li, Tingting" sort="Li, Tingting" uniqKey="Li T" first="Tingting" last="Li">Tingting Li</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling</wicri:regionArea><wicri:noRegion>Yangling</wicri:noRegion></affiliation></author><author><name sortKey="Meng, Yuling" sort="Meng, Yuling" uniqKey="Meng Y" first="Yuling" last="Meng">Yuling Meng</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling</wicri:regionArea><wicri:noRegion>Yangling</wicri:noRegion></affiliation></author><author><name sortKey="Shan, Weixing" sort="Shan, Weixing" uniqKey="Shan W" first="Weixing" last="Shan">Weixing Shan</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling</wicri:regionArea><wicri:noRegion>Yangling</wicri:noRegion></affiliation></author></analytic><series><title level="j">Molecular plant pathology</title><idno type="eISSN">1364-3703</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">Phytophthora species are destructive plant pathogens that cause significant crop losses worldwide. To understand plant susceptibility to oomycete pathogens and to explore novel disease resistance strategies, we employed the Arabidopsis thaliana-Phytophthora parasitica model pathosystem and screened for A. thaliana T-DNA insertion mutant lines resistant to P. parasitica. This led to the identification of the resistant mutant 267-31, which carries two T-DNA insertion sites in the promoter region of the ethylene-responsive factor 19 gene (ERF019). Quantitative reverse transcription PCR (RT-qPCR) assays showed that the expression of ERF019 was induced during P. parasitica infection in the wild type, which was suppressed in the 267-31 mutant. Additional erf019 mutants were generated using CRISPR/Cas9 technology and were confirmed to have increased resistance to P. parasitica. In contrast, ERF019 overexpression lines were more susceptible. Transient overexpression assays in Nicotiana benthamiana showed that the nuclear localization of ERF019 is crucial for its susceptible function. RT-qPCR analyses showed that the expression of marker genes for multiple defence pathways was significantly up-regulated in the mutant compared with the wild type during infection. Flg22-induced hydrogen peroxide accumulation and reactive oxygen species burst were impaired in ERF019 overexpression lines, and flg22-induced MAPK activation was enhanced in erf019 mutants. Moreover, transient overexpression of ERF019 strongly suppressed INF-triggered cell death in N. benthamiana. These results reveal the importance of ERF019 in mediating plant susceptibility to P. parasitica through suppression of pathogen-associated molecular pattern-triggered immunity.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32725756</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>02</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1364-3703</ISSN><JournalIssue CitedMedium="Internet"><Volume>21</Volume><Issue>9</Issue><PubDate><Year>2020</Year><Month>09</Month></PubDate></JournalIssue><Title>Molecular plant pathology</Title><ISOAbbreviation>Mol Plant Pathol</ISOAbbreviation></Journal><ArticleTitle>The Arabidopsis thaliana gene AtERF019 negatively regulates plant resistance to Phytophthora parasitica by suppressing PAMP-triggered immunity.</ArticleTitle><Pagination><MedlinePgn>1179-1193</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1111/mpp.12971</ELocationID><Abstract><AbstractText>Phytophthora species are destructive plant pathogens that cause significant crop losses worldwide. To understand plant susceptibility to oomycete pathogens and to explore novel disease resistance strategies, we employed the Arabidopsis thaliana-Phytophthora parasitica model pathosystem and screened for A. thaliana T-DNA insertion mutant lines resistant to P. parasitica. This led to the identification of the resistant mutant 267-31, which carries two T-DNA insertion sites in the promoter region of the ethylene-responsive factor 19 gene (ERF019). Quantitative reverse transcription PCR (RT-qPCR) assays showed that the expression of ERF019 was induced during P. parasitica infection in the wild type, which was suppressed in the 267-31 mutant. Additional erf019 mutants were generated using CRISPR/Cas9 technology and were confirmed to have increased resistance to P. parasitica. In contrast, ERF019 overexpression lines were more susceptible. Transient overexpression assays in Nicotiana benthamiana showed that the nuclear localization of ERF019 is crucial for its susceptible function. RT-qPCR analyses showed that the expression of marker genes for multiple defence pathways was significantly up-regulated in the mutant compared with the wild type during infection. Flg22-induced hydrogen peroxide accumulation and reactive oxygen species burst were impaired in ERF019 overexpression lines, and flg22-induced MAPK activation was enhanced in erf019 mutants. Moreover, transient overexpression of ERF019 strongly suppressed INF-triggered cell death in N. benthamiana. These results reveal the importance of ERF019 in mediating plant susceptibility to P. parasitica through suppression of pathogen-associated molecular pattern-triggered immunity.</AbstractText><CopyrightInformation>© 2020 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Lu</LastName><ForeName>Wenqin</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Deng</LastName><ForeName>Fengyan</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Life Sciences, Northwest A&F University, Yangling, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jia</LastName><ForeName>Jinbu</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Institute of Plant and Food Science, Department of Biology, Southern University of Science and Technology, Shenzhen, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Xiaokang</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Horticulture, Northwest A&F University, Yangling, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Jinfang</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wen</LastName><ForeName>Qujiang</ForeName><Initials>Q</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Plant Protection, Northwest A&F University, Yangling, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Tingting</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Meng</LastName><ForeName>Yuling</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shan</LastName><ForeName>Weixing</ForeName><Initials>W</Initials><Identifier Source="ORCID">0000-0001-7286-4041</Identifier><AffiliationInfo><Affiliation>State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>07</Month><Day>28</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Mol Plant Pathol</MedlineTA><NlmUniqueID>100954969</NlmUniqueID><ISSNLinking>1364-3703</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Arabidopsis thaliana
</Keyword><Keyword MajorTopicYN="Y">Phytophthora parasitica
</Keyword><Keyword MajorTopicYN="Y">oomycete</Keyword><Keyword MajorTopicYN="Y">susceptibility</Keyword><Keyword MajorTopicYN="Y">transcription factor</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>01</Month><Day>22</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>06</Month><Day>11</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>06</Month><Day>12</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>7</Month><Day>30</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>7</Month><Day>30</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>7</Month><Day>30</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId 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