An RXLR effector PlAvh142 from Peronophythora litchii triggers plant cell death and contributes to virulence.
Identifieur interne : 000304 ( Main/Exploration ); précédent : 000303; suivant : 000305An RXLR effector PlAvh142 from Peronophythora litchii triggers plant cell death and contributes to virulence.
Auteurs : Junjian Situ [République populaire de Chine] ; Liqun Jiang [République populaire de Chine] ; Xiaoning Fan [République populaire de Chine] ; Wensheng Yang [République populaire de Chine] ; Wen Li [République populaire de Chine] ; Pinggen Xi [République populaire de Chine] ; Yizhen Deng [République populaire de Chine] ; Guanghui Kong [République populaire de Chine] ; Zide Jiang [République populaire de Chine]Source :
- Molecular plant pathology [ 1364-3703 ] ; 2020.
Abstract
Litchi downy blight, caused by the phytopathogenic oomycete Peronophythora litchii, results in tremendous economic loss in litchi production every year. To successfully colonize the host cell, Phytophthora species secret hundreds of RXLR effectors that interfere with plant immunity and facilitate the infection process. Previous work has already predicted 245 candidate RXLR effector-encoding genes in P. litchii, 212 of which have been cloned and tested for plant cell death-inducing activity in this study. We found three such RXLR effectors could trigger plant cell death through transient expression in Nicotiana benthamiana. Further experiments demonstrated that PlAvh142 could induce cell death and immune responses in several plants. We also found that PlAvh142 localized in both the cytoplasm and nucleus of plant cells. The cytoplasmic localization was critical for its cell death-inducing activity. Moreover, deletion either of the two internal repeats in PlAvh142 abolished the cell death-inducing activity. Virus-induced gene silencing assays showed that cell death triggered by PlAvh142 was dependent on the plant transduction components RAR1 (require for Mla12 resistance), SGT1 (suppressor of the G2 allele of skp1) and HSP90 (heat shock protein 90). Finally, knockout of PlAvh142 resulted in significantly attenuated P. litchii virulence on litchi plants, whereas the PlAvh142-overexpressed mutants were more aggressive. These data indicated that PlAvh142 could be recognized in plant cytoplasm and is an important virulence RXLR effector of P. litchii.
DOI: 10.1111/mpp.12905
PubMed: 31912634
PubMed Central: PMC7036370
Affiliations:
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last="Kong">Guanghui Kong</name><affiliation wicri:level="3"><nlm:affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou</wicri:regionArea><placeName><settlement type="city">Jiangmen</settlement><region type="province">Guangdong</region></placeName></affiliation></author><author><name sortKey="Jiang, Zide" sort="Jiang, Zide" uniqKey="Jiang Z" first="Zide" last="Jiang">Zide Jiang</name><affiliation wicri:level="3"><nlm:affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</nlm:affiliation><country 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type="wicri:Area/Main/Exploration">000303</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">An RXLR effector PlAvh142 from Peronophythora litchii triggers plant cell death and contributes to virulence.</title><author><name sortKey="Situ, Junjian" sort="Situ, Junjian" uniqKey="Situ J" first="Junjian" last="Situ">Junjian Situ</name><affiliation wicri:level="3"><nlm:affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou</wicri:regionArea><placeName><settlement type="city">Jiangmen</settlement><region type="province">Guangdong</region></placeName></affiliation></author><author><name sortKey="Jiang, Liqun" sort="Jiang, Liqun" uniqKey="Jiang L" first="Liqun" last="Jiang">Liqun Jiang</name><affiliation wicri:level="3"><nlm:affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou</wicri:regionArea><placeName><settlement type="city">Jiangmen</settlement><region type="province">Guangdong</region></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Guangdong Province Key Laboratory of New Technology in Rice Breeding/Rice Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Guangdong Province Key Laboratory of New Technology in Rice Breeding/Rice Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou</wicri:regionArea><placeName><settlement type="city">Jiangmen</settlement><region type="province">Guangdong</region></placeName></affiliation></author><author><name sortKey="Fan, Xiaoning" sort="Fan, Xiaoning" uniqKey="Fan X" first="Xiaoning" last="Fan">Xiaoning Fan</name><affiliation wicri:level="3"><nlm:affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou</wicri:regionArea><placeName><settlement type="city">Jiangmen</settlement><region type="province">Guangdong</region></placeName></affiliation></author><author><name sortKey="Yang, Wensheng" sort="Yang, Wensheng" uniqKey="Yang W" first="Wensheng" last="Yang">Wensheng Yang</name><affiliation wicri:level="3"><nlm:affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou</wicri:regionArea><placeName><settlement type="city">Jiangmen</settlement><region type="province">Guangdong</region></placeName></affiliation></author><author><name sortKey="Li, Wen" sort="Li, Wen" uniqKey="Li W" first="Wen" last="Li">Wen Li</name><affiliation wicri:level="3"><nlm:affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou</wicri:regionArea><placeName><settlement type="city">Jiangmen</settlement><region type="province">Guangdong</region></placeName></affiliation></author><author><name sortKey="Xi, Pinggen" sort="Xi, Pinggen" uniqKey="Xi P" first="Pinggen" last="Xi">Pinggen Xi</name><affiliation wicri:level="3"><nlm:affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou</wicri:regionArea><placeName><settlement type="city">Jiangmen</settlement><region type="province">Guangdong</region></placeName></affiliation></author><author><name sortKey="Deng, Yizhen" sort="Deng, Yizhen" uniqKey="Deng Y" first="Yizhen" last="Deng">Yizhen Deng</name><affiliation wicri:level="3"><nlm:affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou</wicri:regionArea><placeName><settlement type="city">Jiangmen</settlement><region type="province">Guangdong</region></placeName></affiliation></author><author><name sortKey="Kong, Guanghui" sort="Kong, Guanghui" uniqKey="Kong G" first="Guanghui" last="Kong">Guanghui Kong</name><affiliation wicri:level="3"><nlm:affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou</wicri:regionArea><placeName><settlement type="city">Jiangmen</settlement><region type="province">Guangdong</region></placeName></affiliation></author><author><name sortKey="Jiang, Zide" sort="Jiang, Zide" uniqKey="Jiang Z" first="Zide" last="Jiang">Zide Jiang</name><affiliation wicri:level="3"><nlm:affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou</wicri:regionArea><placeName><settlement type="city">Jiangmen</settlement><region type="province">Guangdong</region></placeName></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">Litchi downy blight, caused by the phytopathogenic oomycete Peronophythora litchii, results in tremendous economic loss in litchi production every year. To successfully colonize the host cell, Phytophthora species secret hundreds of RXLR effectors that interfere with plant immunity and facilitate the infection process. Previous work has already predicted 245 candidate RXLR effector-encoding genes in P. litchii, 212 of which have been cloned and tested for plant cell death-inducing activity in this study. We found three such RXLR effectors could trigger plant cell death through transient expression in Nicotiana benthamiana. Further experiments demonstrated that PlAvh142 could induce cell death and immune responses in several plants. We also found that PlAvh142 localized in both the cytoplasm and nucleus of plant cells. The cytoplasmic localization was critical for its cell death-inducing activity. Moreover, deletion either of the two internal repeats in PlAvh142 abolished the cell death-inducing activity. Virus-induced gene silencing assays showed that cell death triggered by PlAvh142 was dependent on the plant transduction components RAR1 (require for Mla12 resistance), SGT1 (suppressor of the G2 allele of skp1) and HSP90 (heat shock protein 90). Finally, knockout of PlAvh142 resulted in significantly attenuated P. litchii virulence on litchi plants, whereas the PlAvh142-overexpressed mutants were more aggressive. These data indicated that PlAvh142 could be recognized in plant cytoplasm and is an important virulence RXLR effector of P. litchii.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">31912634</PMID><DateRevised><Year>2020</Year><Month>04</Month><Day>20</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1364-3703</ISSN><JournalIssue CitedMedium="Internet"><Volume>21</Volume><Issue>3</Issue><PubDate><Year>2020</Year><Month>03</Month></PubDate></JournalIssue><Title>Molecular plant pathology</Title><ISOAbbreviation>Mol Plant Pathol</ISOAbbreviation></Journal><ArticleTitle>An RXLR effector PlAvh142 from Peronophythora litchii triggers plant cell death and contributes to virulence.</ArticleTitle><Pagination><MedlinePgn>415-428</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1111/mpp.12905</ELocationID><Abstract><AbstractText>Litchi downy blight, caused by the phytopathogenic oomycete Peronophythora litchii, results in tremendous economic loss in litchi production every year. To successfully colonize the host cell, Phytophthora species secret hundreds of RXLR effectors that interfere with plant immunity and facilitate the infection process. Previous work has already predicted 245 candidate RXLR effector-encoding genes in P. litchii, 212 of which have been cloned and tested for plant cell death-inducing activity in this study. We found three such RXLR effectors could trigger plant cell death through transient expression in Nicotiana benthamiana. Further experiments demonstrated that PlAvh142 could induce cell death and immune responses in several plants. We also found that PlAvh142 localized in both the cytoplasm and nucleus of plant cells. The cytoplasmic localization was critical for its cell death-inducing activity. Moreover, deletion either of the two internal repeats in PlAvh142 abolished the cell death-inducing activity. Virus-induced gene silencing assays showed that cell death triggered by PlAvh142 was dependent on the plant transduction components RAR1 (require for Mla12 resistance), SGT1 (suppressor of the G2 allele of skp1) and HSP90 (heat shock protein 90). Finally, knockout of PlAvh142 resulted in significantly attenuated P. litchii virulence on litchi plants, whereas the PlAvh142-overexpressed mutants were more aggressive. These data indicated that PlAvh142 could be recognized in plant cytoplasm and is an important virulence RXLR effector of P. litchii.</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>Situ</LastName><ForeName>Junjian</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jiang</LastName><ForeName>Liqun</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Guangdong Province Key Laboratory of New Technology in Rice Breeding/Rice Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fan</LastName><ForeName>Xiaoning</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yang</LastName><ForeName>Wensheng</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Wen</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xi</LastName><ForeName>Pinggen</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Deng</LastName><ForeName>Yizhen</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kong</LastName><ForeName>Guanghui</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jiang</LastName><ForeName>Zide</ForeName><Initials>Z</Initials><Identifier Source="ORCID">0000-0002-1274-4627</Identifier><AffiliationInfo><Affiliation>Department of Plant Pathology/Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou, 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>01</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="Y">Peronophythora litchii
</Keyword><Keyword MajorTopicYN="Y">RXLR effector</Keyword><Keyword MajorTopicYN="Y">cell death</Keyword><Keyword MajorTopicYN="Y">plant immunity</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>07</Month><Day>17</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2019</Year><Month>12</Month><Day>05</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>12</Month><Day>06</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>1</Month><Day>9</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>1</Month><Day>9</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>1</Month><Day>9</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId 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