Establishment of a novel virus-induced virulence effector assay for the identification of virulence effectors of plant pathogens using a PVX-based expression vector.
Identifieur interne : 000176 ( Main/Exploration ); précédent : 000175; suivant : 000177Establishment of a novel virus-induced virulence effector assay for the identification of virulence effectors of plant pathogens using a PVX-based expression vector.
Auteurs : Jinxia Shi [République populaire de Chine] ; Yuanhong Zhu [République populaire de Chine] ; Ming Li [République populaire de Chine] ; Yuqing Ma [République populaire de Chine] ; Huarong Liu [République populaire de Chine] ; Peng Zhang [République populaire de Chine] ; Di Fang ; Yushuang Guo [République populaire de Chine] ; Ping Xu [République populaire de Chine] ; Yongli Qiao [République populaire de Chine]Source :
- Molecular plant pathology [ 1364-3703 ] ; 2020.
Abstract
Plant pathogens deliver virulence effectors into plant cells to modulate plant immunity and facilitate infection. Although species-specific virulence effector screening approaches have been developed for several pathogens, these assays do not apply to pathogens that cannot be cultured and/or transformed outside of their hosts. Here, we established a rapid and parallel screening assay, called the virus-induced virulence effector (VIVE) assay, to identify putative effectors in various plant pathogens, including unculturable pathogens, using a virus-based expression vector. The VIVE assay uses the potato virus X (PVX) vector to transiently express candidate effector genes of various bacterial and fungal pathogens into Nicotiana benthamiana leaves. Using the VIVE assay, we successfully identified Avh148 as a potential virulence effector of Phytophthora sojae. Plants infected with PVX carrying Avh148 showed strong viral symptoms and high-level Avh148 and viral RNA accumulation. Analysis of P. sojae Avh148 deletion mutants and soybean hairy roots overexpressing Avh148 revealed that Avh148 is required for full pathogen virulence. In addition, the VIVE assay was optimized in N. benthamiana plants at different developmental stages across a range of Agrobacterium cell densities. Overall, we identified six novel virulence effectors from seven pathogens, thus demonstrating the broad effectiveness of the VIVE assay in plant pathology research.
DOI: 10.1111/mpp.13000
PubMed: 33029873
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Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation></author><author><name sortKey="Li, Ming" sort="Li, Ming" uniqKey="Li M" first="Ming" last="Li">Ming Li</name><affiliation wicri:level="1"><nlm:affiliation>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation></author><author><name sortKey="Ma, 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Jingzhou</wicri:regionArea><wicri:noRegion>Jingzhou</wicri:noRegion></affiliation></author><author><name sortKey="Fang, Di" sort="Fang, Di" uniqKey="Fang D" first="Di" last="Fang">Di Fang</name></author><author><name sortKey="Guo, Yushuang" sort="Guo, Yushuang" uniqKey="Guo Y" first="Yushuang" last="Guo">Yushuang Guo</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Molecular Genetics, China National Tobacco Corporation, Guizhou Institute of Tobacco Science, Guiyang, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Laboratory of Molecular Genetics, China National Tobacco Corporation, Guizhou Institute of Tobacco Science, Guiyang</wicri:regionArea><wicri:noRegion>Guiyang</wicri:noRegion></affiliation></author><author><name sortKey="Xu, Ping" sort="Xu, Ping" uniqKey="Xu P" first="Ping" last="Xu">Ping Xu</name><affiliation wicri:level="1"><nlm:affiliation>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation></author><author><name sortKey="Qiao, Yongli" sort="Qiao, Yongli" uniqKey="Qiao Y" first="Yongli" last="Qiao">Yongli Qiao</name><affiliation wicri:level="1"><nlm:affiliation>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno 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Sciences, Shanghai Normal University, Shanghai, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation></author><author><name sortKey="Zhu, Yuanhong" sort="Zhu, Yuanhong" uniqKey="Zhu Y" first="Yuanhong" last="Zhu">Yuanhong Zhu</name><affiliation wicri:level="1"><nlm:affiliation>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation></author><author><name sortKey="Li, Ming" sort="Li, Ming" uniqKey="Li M" first="Ming" last="Li">Ming Li</name><affiliation wicri:level="1"><nlm:affiliation>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation></author><author><name sortKey="Ma, Yuqing" sort="Ma, Yuqing" uniqKey="Ma Y" first="Yuqing" last="Ma">Yuqing Ma</name><affiliation wicri:level="1"><nlm:affiliation>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation></author><author><name sortKey="Liu, Huarong" sort="Liu, Huarong" uniqKey="Liu H" first="Huarong" last="Liu">Huarong Liu</name><affiliation wicri:level="1"><nlm:affiliation>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Peng" sort="Zhang, Peng" uniqKey="Zhang P" first="Peng" last="Zhang">Peng Zhang</name><affiliation wicri:level="1"><nlm:affiliation>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>College of Agriculture, Yangtze University, Jingzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Agriculture, Yangtze University, Jingzhou</wicri:regionArea><wicri:noRegion>Jingzhou</wicri:noRegion></affiliation></author><author><name sortKey="Fang, Di" sort="Fang, Di" uniqKey="Fang D" first="Di" last="Fang">Di Fang</name></author><author><name sortKey="Guo, Yushuang" sort="Guo, Yushuang" uniqKey="Guo Y" first="Yushuang" last="Guo">Yushuang Guo</name><affiliation wicri:level="1"><nlm:affiliation>Laboratory of Molecular Genetics, China National Tobacco Corporation, Guizhou Institute of Tobacco Science, Guiyang, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Laboratory of Molecular Genetics, China National Tobacco Corporation, Guizhou Institute of Tobacco Science, Guiyang</wicri:regionArea><wicri:noRegion>Guiyang</wicri:noRegion></affiliation></author><author><name sortKey="Xu, Ping" sort="Xu, Ping" uniqKey="Xu P" first="Ping" last="Xu">Ping Xu</name><affiliation wicri:level="1"><nlm:affiliation>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation></author><author><name sortKey="Qiao, Yongli" sort="Qiao, Yongli" uniqKey="Qiao Y" first="Yongli" last="Qiao">Yongli Qiao</name><affiliation wicri:level="1"><nlm:affiliation>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</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">Plant pathogens deliver virulence effectors into plant cells to modulate plant immunity and facilitate infection. Although species-specific virulence effector screening approaches have been developed for several pathogens, these assays do not apply to pathogens that cannot be cultured and/or transformed outside of their hosts. Here, we established a rapid and parallel screening assay, called the virus-induced virulence effector (VIVE) assay, to identify putative effectors in various plant pathogens, including unculturable pathogens, using a virus-based expression vector. The VIVE assay uses the potato virus X (PVX) vector to transiently express candidate effector genes of various bacterial and fungal pathogens into Nicotiana benthamiana leaves. Using the VIVE assay, we successfully identified Avh148 as a potential virulence effector of Phytophthora sojae. Plants infected with PVX carrying Avh148 showed strong viral symptoms and high-level Avh148 and viral RNA accumulation. Analysis of P. sojae Avh148 deletion mutants and soybean hairy roots overexpressing Avh148 revealed that Avh148 is required for full pathogen virulence. In addition, the VIVE assay was optimized in N. benthamiana plants at different developmental stages across a range of Agrobacterium cell densities. Overall, we identified six novel virulence effectors from seven pathogens, thus demonstrating the broad effectiveness of the VIVE assay in plant pathology research.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">33029873</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>10</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1364-3703</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Oct</Month><Day>07</Day></PubDate></JournalIssue><Title>Molecular plant pathology</Title><ISOAbbreviation>Mol Plant Pathol</ISOAbbreviation></Journal><ArticleTitle>Establishment of a novel virus-induced virulence effector assay for the identification of virulence effectors of plant pathogens using a PVX-based expression vector.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1111/mpp.13000</ELocationID><Abstract><AbstractText>Plant pathogens deliver virulence effectors into plant cells to modulate plant immunity and facilitate infection. Although species-specific virulence effector screening approaches have been developed for several pathogens, these assays do not apply to pathogens that cannot be cultured and/or transformed outside of their hosts. Here, we established a rapid and parallel screening assay, called the virus-induced virulence effector (VIVE) assay, to identify putative effectors in various plant pathogens, including unculturable pathogens, using a virus-based expression vector. The VIVE assay uses the potato virus X (PVX) vector to transiently express candidate effector genes of various bacterial and fungal pathogens into Nicotiana benthamiana leaves. Using the VIVE assay, we successfully identified Avh148 as a potential virulence effector of Phytophthora sojae. Plants infected with PVX carrying Avh148 showed strong viral symptoms and high-level Avh148 and viral RNA accumulation. Analysis of P. sojae Avh148 deletion mutants and soybean hairy roots overexpressing Avh148 revealed that Avh148 is required for full pathogen virulence. In addition, the VIVE assay was optimized in N. benthamiana plants at different developmental stages across a range of Agrobacterium cell densities. Overall, we identified six novel virulence effectors from seven pathogens, thus demonstrating the broad effectiveness of the VIVE assay in plant pathology research.</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>Shi</LastName><ForeName>Jinxia</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhu</LastName><ForeName>Yuanhong</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Ming</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ma</LastName><ForeName>Yuqing</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Huarong</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Peng</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>College of Agriculture, Yangtze University, Jingzhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fang</LastName><ForeName>Di</ForeName><Initials>D</Initials></Author><Author ValidYN="Y"><LastName>Guo</LastName><ForeName>Yushuang</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Laboratory of Molecular Genetics, China National Tobacco Corporation, Guizhou Institute of Tobacco Science, Guiyang, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xu</LastName><ForeName>Ping</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Qiao</LastName><ForeName>Yongli</ForeName><Initials>Y</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-9178-5293</Identifier><AffiliationInfo><Affiliation>Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>18DZ2260500</GrantID><Agency>the Science and Technology Commission of Shanghai Municipality</Agency><Country></Country></Grant><Grant><GrantID>2018YFD0201500</GrantID><Agency>the National Key Research and Development Program of China National Key R&D Program of China</Agency><Country></Country></Grant><Grant><Agency>the Thousand Talents Program for Young Professionals of China</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>10</Month><Day>07</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="N">Nicotiana benthamiana
</Keyword><Keyword MajorTopicYN="N">PVX</Keyword><Keyword MajorTopicYN="N">plant pathogens</Keyword><Keyword MajorTopicYN="N">screening assay</Keyword><Keyword MajorTopicYN="N">virulence effector</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>04</Month><Day>29</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>08</Month><Day>31</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>09</Month><Day>04</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>10</Month><Day>9</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>10</Month><Day>9</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>10</Month><Day>8</Day><Hour>5</Hour><Minute>37</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">33029873</ArticleId><ArticleId IdType="doi">10.1111/mpp.13000</ArticleId></ArticleIdList><ReferenceList><Title>REFERENCES</Title><Reference><Citation>Baulcombe, D. 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