In Planta Functional Analysis and Subcellular Localization of the Oomycete Pathogen Plasmopara viticola Candidate RXLR Effector Repertoire.
Identifieur interne : 000288 ( Main/Exploration ); précédent : 000287; suivant : 000289In Planta Functional Analysis and Subcellular Localization of the Oomycete Pathogen Plasmopara viticola Candidate RXLR Effector Repertoire.
Auteurs : Yunxiao Liu [République populaire de Chine] ; Xia Lan [République populaire de Chine] ; Shiren Song [République populaire de Chine] ; Ling Yin [République populaire de Chine] ; Ian B. Dry [Australie] ; Junjie Qu [République populaire de Chine] ; Jiang Xiang [République populaire de Chine] ; Jiang Lu [République populaire de Chine]Source :
- Frontiers in plant science [ 1664-462X ] ; 2018.
Abstract
Downy mildew is one of the most destructive diseases of grapevine, causing tremendous economic loss in the grape and wine industry. The disease agent Plasmopara viticola is an obligate biotrophic oomycete, from which over 100 candidate RXLR effectors have been identified. In this study, 83 candidate RXLR effector genes (PvRXLRs) were cloned from the P. viticola isolate "JL-7-2" genome. The results of the yeast signal sequence trap assay indicated that most of the candidate effectors are secretory proteins. The biological activities and subcellular localizations of all the 83 effectors were analyzed via a heterologous Agrobacterium-mediated Nicotiana benthamiana expression system. Results showed that 52 effectors could completely suppress cell death triggered by elicitin, 10 effectors could partially suppress cell death, 11 effectors were unable to suppress cell death, and 10 effectors themselves triggered cell death. Live-cell imaging showed that the majority of the effectors (76 of 83) could be observed with informative fluorescence signals in plant cells, among which 34 effectors were found to be targeted to both the nucleus and cytosol, 29 effectors were specifically localized in the nucleus, and 9 effectors were targeted to plant membrane system. Interestingly, three effectors PvRXLR61, 86 and 161 were targeted to chloroplasts, and one effector PvRXLR54 was dually targeted to chloroplasts and mitochondria. However, western blot analysis suggested that only PvRXLR86 carried a cleavable N-terminal transit peptide and underwent processing in planta. Many effectors have previously been predicted to target organelles, however, to the best of our knowledge, this is the first study to provide experimental evidence of oomycete effectors targeted to chloroplasts and mitochondria.
DOI: 10.3389/fpls.2018.00286
PubMed: 29706971
PubMed Central: PMC5908963
Affiliations:
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L" first="Ling" last="Yin">Ling Yin</name><affiliation wicri:level="1"><nlm:affiliation>Guangxi Crop Genetic Improvement and Biotechnology Laboratory, Guangxi Academy of Agricultural Sciences, Nanning, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Guangxi Crop Genetic Improvement and Biotechnology Laboratory, Guangxi Academy of Agricultural Sciences, Nanning</wicri:regionArea><wicri:noRegion>Nanning</wicri:noRegion></affiliation></author><author><name sortKey="Dry, Ian B" sort="Dry, Ian B" uniqKey="Dry I" first="Ian B" last="Dry">Ian B. Dry</name><affiliation wicri:level="1"><nlm:affiliation>CSIRO Agriculture & Food, Urrbrae, SA, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>CSIRO Agriculture & Food, Urrbrae, SA</wicri:regionArea><wicri:noRegion>SA</wicri:noRegion></affiliation></author><author><name sortKey="Qu, Junjie" sort="Qu, Junjie" uniqKey="Qu J" first="Junjie" last="Qu">Junjie Qu</name><affiliation wicri:level="1"><nlm:affiliation>Guangxi Crop Genetic Improvement and Biotechnology Laboratory, Guangxi Academy of Agricultural Sciences, Nanning, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Guangxi Crop Genetic Improvement and Biotechnology Laboratory, Guangxi Academy of Agricultural Sciences, Nanning</wicri:regionArea><wicri:noRegion>Nanning</wicri:noRegion></affiliation></author><author><name sortKey="Xiang, Jiang" sort="Xiang, Jiang" uniqKey="Xiang J" first="Jiang" last="Xiang">Jiang Xiang</name><affiliation wicri:level="1"><nlm:affiliation>Center for Viticulture and Enology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Center for Viticulture and Enology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation></author><author><name sortKey="Lu, Jiang" sort="Lu, Jiang" uniqKey="Lu J" first="Jiang" last="Lu">Jiang Lu</name><affiliation wicri:level="1"><nlm:affiliation>Center for Viticulture and Enology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Center for Viticulture and Enology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai</wicri:regionArea><wicri:noRegion>Shanghai</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Guangxi Crop Genetic Improvement and Biotechnology Laboratory, Guangxi Academy of Agricultural Sciences, Nanning, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Guangxi Crop Genetic Improvement and Biotechnology Laboratory, Guangxi Academy of Agricultural Sciences, Nanning</wicri:regionArea><wicri:noRegion>Nanning</wicri:noRegion></affiliation></author></analytic><series><title level="j">Frontiers in plant science</title><idno type="ISSN">1664-462X</idno><imprint><date when="2018" type="published">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Downy mildew is one of the most destructive diseases of grapevine, causing tremendous economic loss in the grape and wine industry. The disease agent <i>Plasmopara viticola</i> is an obligate biotrophic oomycete, from which over 100 candidate RXLR effectors have been identified. In this study, 83 candidate RXLR effector genes (<i>PvRXLRs</i>) were cloned from the <i>P. viticola</i> isolate "JL-7-2" genome. The results of the yeast signal sequence trap assay indicated that most of the candidate effectors are secretory proteins. The biological activities and subcellular localizations of all the 83 effectors were analyzed via a heterologous <i>Agrobacterium</i>-mediated <i>Nicotiana benthamiana</i> expression system. Results showed that 52 effectors could completely suppress cell death triggered by elicitin, 10 effectors could partially suppress cell death, 11 effectors were unable to suppress cell death, and 10 effectors themselves triggered cell death. Live-cell imaging showed that the majority of the effectors (76 of 83) could be observed with informative fluorescence signals in plant cells, among which 34 effectors were found to be targeted to both the nucleus and cytosol, 29 effectors were specifically localized in the nucleus, and 9 effectors were targeted to plant membrane system. Interestingly, three effectors PvRXLR61, 86 and 161 were targeted to chloroplasts, and one effector PvRXLR54 was dually targeted to chloroplasts and mitochondria. However, western blot analysis suggested that only PvRXLR86 carried a cleavable <i>N</i>-terminal transit peptide and underwent processing <i>in planta</i>. Many effectors have previously been predicted to target organelles, however, to the best of our knowledge, this is the first study to provide experimental evidence of oomycete effectors targeted to chloroplasts and mitochondria.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">29706971</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>30</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-462X</ISSN><JournalIssue CitedMedium="Print"><Volume>9</Volume><PubDate><Year>2018</Year></PubDate></JournalIssue><Title>Frontiers in plant science</Title><ISOAbbreviation>Front Plant Sci</ISOAbbreviation></Journal><ArticleTitle><i>In Planta</i> Functional Analysis and Subcellular Localization of the Oomycete Pathogen <i>Plasmopara viticola</i> Candidate RXLR Effector Repertoire.</ArticleTitle><Pagination><MedlinePgn>286</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fpls.2018.00286</ELocationID><Abstract><AbstractText>Downy mildew is one of the most destructive diseases of grapevine, causing tremendous economic loss in the grape and wine industry. The disease agent <i>Plasmopara viticola</i> is an obligate biotrophic oomycete, from which over 100 candidate RXLR effectors have been identified. In this study, 83 candidate RXLR effector genes (<i>PvRXLRs</i>) were cloned from the <i>P. viticola</i> isolate "JL-7-2" genome. The results of the yeast signal sequence trap assay indicated that most of the candidate effectors are secretory proteins. The biological activities and subcellular localizations of all the 83 effectors were analyzed via a heterologous <i>Agrobacterium</i>-mediated <i>Nicotiana benthamiana</i> expression system. Results showed that 52 effectors could completely suppress cell death triggered by elicitin, 10 effectors could partially suppress cell death, 11 effectors were unable to suppress cell death, and 10 effectors themselves triggered cell death. Live-cell imaging showed that the majority of the effectors (76 of 83) could be observed with informative fluorescence signals in plant cells, among which 34 effectors were found to be targeted to both the nucleus and cytosol, 29 effectors were specifically localized in the nucleus, and 9 effectors were targeted to plant membrane system. Interestingly, three effectors PvRXLR61, 86 and 161 were targeted to chloroplasts, and one effector PvRXLR54 was dually targeted to chloroplasts and mitochondria. However, western blot analysis suggested that only PvRXLR86 carried a cleavable <i>N</i>-terminal transit peptide and underwent processing <i>in planta</i>. Many effectors have previously been predicted to target organelles, however, to the best of our knowledge, this is the first study to provide experimental evidence of oomycete effectors targeted to chloroplasts and mitochondria.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Liu</LastName><ForeName>Yunxiao</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>College of Food Science and Nutritional Engineering, China Agricultural University, Beijing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Center for Viticulture and Enology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lan</LastName><ForeName>Xia</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>College of Food Science and Nutritional Engineering, China Agricultural University, Beijing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Center for Viticulture and Enology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Song</LastName><ForeName>Shiren</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Center for Viticulture and Enology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yin</LastName><ForeName>Ling</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Guangxi Crop Genetic Improvement and Biotechnology Laboratory, Guangxi Academy of Agricultural Sciences, Nanning, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dry</LastName><ForeName>Ian B</ForeName><Initials>IB</Initials><AffiliationInfo><Affiliation>CSIRO Agriculture & Food, Urrbrae, SA, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Qu</LastName><ForeName>Junjie</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Guangxi Crop Genetic Improvement and Biotechnology Laboratory, Guangxi Academy of Agricultural Sciences, Nanning, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xiang</LastName><ForeName>Jiang</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Center for Viticulture and Enology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lu</LastName><ForeName>Jiang</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Center for Viticulture and Enology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Guangxi Crop Genetic Improvement and Biotechnology Laboratory, Guangxi Academy of Agricultural Sciences, Nanning, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2018</Year><Month>04</Month><Day>13</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Plant Sci</MedlineTA><NlmUniqueID>101568200</NlmUniqueID><ISSNLinking>1664-462X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Plasmopara viticola</Keyword><Keyword MajorTopicYN="N">RXLR effectors</Keyword><Keyword MajorTopicYN="N">chloroplast</Keyword><Keyword MajorTopicYN="N">dual-targeting</Keyword><Keyword MajorTopicYN="N">function</Keyword><Keyword MajorTopicYN="N">localization</Keyword><Keyword MajorTopicYN="N">mitochondria</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2017</Year><Month>10</Month><Day>04</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2018</Year><Month>02</Month><Day>19</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2018</Year><Month>5</Month><Day>1</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2018</Year><Month>5</Month><Day>1</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2018</Year><Month>5</Month><Day>1</Day><Hour>6</Hour><Minute>1</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">29706971</ArticleId><ArticleId IdType="doi">10.3389/fpls.2018.00286</ArticleId><ArticleId IdType="pmc">PMC5908963</ArticleId></ArticleIdList><ReferenceList><Reference><Citation>PLoS Genet. 2013 Jun;9(6):e1003272</Citation><ArticleIdList><ArticleId IdType="pubmed">23785293</ArticleId></ArticleIdList></Reference><Reference><Citation>Mol 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