Phosphorylation of ATG18a by BAK1 suppresses autophagy and attenuates plant resistance against necrotrophic pathogens.
Identifieur interne : 000085 ( Main/Exploration ); précédent : 000084; suivant : 000086Phosphorylation of ATG18a by BAK1 suppresses autophagy and attenuates plant resistance against necrotrophic pathogens.
Auteurs : Bao Zhang [République populaire de Chine] ; Lu Shao [République populaire de Chine] ; Jiali Wang [République populaire de Chine] ; Yan Zhang [République populaire de Chine] ; Xiaoshuang Guo [République populaire de Chine] ; Yujiao Peng [République populaire de Chine] ; Yangrong Cao [République populaire de Chine] ; Zhibing Lai [République populaire de Chine]Source :
- Autophagy [ 1554-8635 ] ; 2020.
Abstract
Autophagy is critical for plant defense against necrotrophic pathogens, which causes serious yield loss on crops. However, the post-translational regulatory mechanisms of autophagy pathway in plant resistance against necrotrophs remain poorly understood. In this study, we report that phosphorylation modification on ATG18a, a key regulator of autophagosome formation in Arabidopsis thaliana, constitutes a post-translation regulation of autophagy, which attenuates plant resistance against necrotrophic pathogens. We found that phosphorylation of ATG18a suppresses autophagosome formation and its subsequent delivery into the vacuole, which results in reduced autophagy activity and compromised plant resistance against Botrytis cinerea. In contrast, overexpression of ATG18a dephosphorylation-mimic form increases the accumulation of autophagosomes and complements the plant resistance of atg18a mutant against B. cinerea. Moreover, BAK1, a key regulator in plant resistance, was identified to physically interact with and phosphorylate ATG18a. Mutation of BAK1 blocks ATG18a phosphorylation at four of the five detected phosphorylation sites after B. cinerea infection and strongly activates autophagy, leading to enhanced resistance against B. cinerea. Collectively, the identification of functional phosphorylation sites on ATG18a and the corresponding kinase BAK1 unveiled how plant regulates autophagy during resistance against necrotrophic pathogens.
ABBREVIATIONS
DOI: 10.1080/15548627.2020.1810426
PubMed: 32804012
Affiliations:
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Chine</country><wicri:regionArea>National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University , Wuhan</wicri:regionArea><placeName><settlement type="city">Wuhan</settlement><region type="région">Hubei</region></placeName></affiliation></author><author><name sortKey="Shao, Lu" sort="Shao, Lu" uniqKey="Shao L" first="Lu" last="Shao">Lu Shao</name><affiliation wicri:level="3"><nlm:affiliation>National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University , Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University , Wuhan</wicri:regionArea><placeName><settlement type="city">Wuhan</settlement><region type="région">Hubei</region></placeName></affiliation></author><author><name sortKey="Wang, Jiali" sort="Wang, Jiali" uniqKey="Wang J" first="Jiali" last="Wang">Jiali Wang</name><affiliation wicri:level="3"><nlm:affiliation>National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University , Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University , Wuhan</wicri:regionArea><placeName><settlement type="city">Wuhan</settlement><region type="région">Hubei</region></placeName></affiliation></author><author><name sortKey="Zhang, Yan" sort="Zhang, Yan" uniqKey="Zhang Y" first="Yan" last="Zhang">Yan Zhang</name><affiliation wicri:level="1"><nlm:affiliation>Ecology College, Lishui University , Lishui, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Ecology College, Lishui University , Lishui</wicri:regionArea><wicri:noRegion>Lishui</wicri:noRegion></affiliation></author><author><name sortKey="Guo, Xiaoshuang" sort="Guo, Xiaoshuang" uniqKey="Guo X" first="Xiaoshuang" last="Guo">Xiaoshuang Guo</name><affiliation wicri:level="3"><nlm:affiliation>National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University , Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University , Wuhan</wicri:regionArea><placeName><settlement type="city">Wuhan</settlement><region type="région">Hubei</region></placeName></affiliation></author><author><name sortKey="Peng, Yujiao" sort="Peng, Yujiao" uniqKey="Peng Y" first="Yujiao" last="Peng">Yujiao Peng</name><affiliation wicri:level="3"><nlm:affiliation>National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University , Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University , Wuhan</wicri:regionArea><placeName><settlement type="city">Wuhan</settlement><region type="région">Hubei</region></placeName></affiliation></author><author><name sortKey="Cao, Yangrong" sort="Cao, Yangrong" uniqKey="Cao Y" first="Yangrong" last="Cao">Yangrong Cao</name><affiliation wicri:level="3"><nlm:affiliation>State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University , Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University , Wuhan</wicri:regionArea><placeName><settlement type="city">Wuhan</settlement><region type="région">Hubei</region></placeName></affiliation></author><author><name sortKey="Lai, Zhibing" sort="Lai, Zhibing" uniqKey="Lai Z" first="Zhibing" last="Lai">Zhibing Lai</name><affiliation wicri:level="3"><nlm:affiliation>National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University , Wuhan, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University , Wuhan</wicri:regionArea><placeName><settlement type="city">Wuhan</settlement><region type="région">Hubei</region></placeName></affiliation></author></analytic><series><title level="j">Autophagy</title><idno type="eISSN">1554-8635</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">Autophagy is critical for plant defense against necrotrophic pathogens, which causes serious yield loss on crops. However, the post-translational regulatory mechanisms of autophagy pathway in plant resistance against necrotrophs remain poorly understood. In this study, we report that phosphorylation modification on ATG18a, a key regulator of autophagosome formation in <i>Arabidopsis thaliana</i>, constitutes a post-translation regulation of autophagy, which attenuates plant resistance against necrotrophic pathogens. We found that phosphorylation of ATG18a suppresses autophagosome formation and its subsequent delivery into the vacuole, which results in reduced autophagy activity and compromised plant resistance against <i>Botrytis cinerea</i>. In contrast, overexpression of ATG18a dephosphorylation-mimic form increases the accumulation of autophagosomes and complements the plant resistance of <i>atg18a</i> mutant against <i>B. cinerea</i>. Moreover, BAK1, a key regulator in plant resistance, was identified to physically interact with and phosphorylate ATG18a. Mutation of <i>BAK1</i> blocks ATG18a phosphorylation at four of the five detected phosphorylation sites after <i>B. cinerea</i> infection and strongly activates autophagy, leading to enhanced resistance against <i>B. cinerea</i>. Collectively, the identification of functional phosphorylation sites on ATG18a and the corresponding kinase BAK1 unveiled how plant regulates autophagy during resistance against necrotrophic pathogens.</div><div type="abstract" xml:lang="en"><p><b>ABBREVIATIONS</b></p><p></p></div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">32804012</PMID><DateRevised><Year>2020</Year><Month>08</Month><Day>26</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1554-8635</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Aug</Month><Day>26</Day></PubDate></JournalIssue><Title>Autophagy</Title><ISOAbbreviation>Autophagy</ISOAbbreviation></Journal><ArticleTitle>Phosphorylation of ATG18a by BAK1 suppresses autophagy and attenuates plant resistance against necrotrophic pathogens.</ArticleTitle><Pagination><MedlinePgn>1-18</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1080/15548627.2020.1810426</ELocationID><Abstract><AbstractText>Autophagy is critical for plant defense against necrotrophic pathogens, which causes serious yield loss on crops. However, the post-translational regulatory mechanisms of autophagy pathway in plant resistance against necrotrophs remain poorly understood. In this study, we report that phosphorylation modification on ATG18a, a key regulator of autophagosome formation in <i>Arabidopsis thaliana</i>, constitutes a post-translation regulation of autophagy, which attenuates plant resistance against necrotrophic pathogens. We found that phosphorylation of ATG18a suppresses autophagosome formation and its subsequent delivery into the vacuole, which results in reduced autophagy activity and compromised plant resistance against <i>Botrytis cinerea</i>. In contrast, overexpression of ATG18a dephosphorylation-mimic form increases the accumulation of autophagosomes and complements the plant resistance of <i>atg18a</i> mutant against <i>B. cinerea</i>. Moreover, BAK1, a key regulator in plant resistance, was identified to physically interact with and phosphorylate ATG18a. Mutation of <i>BAK1</i> blocks ATG18a phosphorylation at four of the five detected phosphorylation sites after <i>B. cinerea</i> infection and strongly activates autophagy, leading to enhanced resistance against <i>B. cinerea</i>. Collectively, the identification of functional phosphorylation sites on ATG18a and the corresponding kinase BAK1 unveiled how plant regulates autophagy during resistance against necrotrophic pathogens.</AbstractText><AbstractText Label="ABBREVIATIONS" NlmCategory="BACKGROUND"><i>35s</i>: the cauliflower mosaic virus <i>35s</i> promoter; <i>A. thaliana: Arabidopsis thaliana; A. brassicicola: Alternaria brassicicola</i>; ABA: abscisic acid; ATG: autophagy-related; ATG18a: autophagy-related protein 18a in <i>A. thaliana</i>; ATG8a: autophagy-related protein 8a in <i>A. thaliana</i>; ATG8-PE: ATG8 conjugated with PE; <i>B. cinerea: Botrytis cinerea</i>; BAK1: Brassinosteroid insensitive 1-associated receptor kinase1 in <i>A. thaliana</i>; BiFC: biomolecular fluorescence complementation; BIK1: Botrytis-insensitive kinase 1 in <i>A. thaliana</i>; BKK1: BAK1-like 1 in <i>A. thaliana</i>; BR: brassinosteroid; Co-IP: coimmunoprecipitation; dai: days after inoculation; DAMPs: damage-associated molecular patterns; <i>E. coli: Escherochia coli</i>; ER: endoplasmic reticulum; ETI: effector-triggered immunity; GFP: green fluorescent protein; HA: hemagglutinin; IP: immunoprecipitation; LC-MS/MS: liquid chromatography-tandem mass spectrometry; LCI: luciferase complementation imaging; MPK3: mitogen-activated protein kinase 3 in <i>A. thaliana</i>; MPK4: mitogen-activated protein kinase 4 in <i>A. thaliana</i>; MPK6: mitogen-activated protein kinase 6 in <i>A. thaliana; N. benthamiana: Nicotiana benthamiana</i>; NES: nuclear export sequence; PAMP: pathogen-associated molecular pattern; PCR: polymerase chain reaction; PE: phosphatidylethanolamine; PRR: pattern recognition receptor; PtdIns(3,5)P<sub>2:</sub> phosphatidylinositol (3,5)-biphosphate; PtdIns3P: phosphatidylinositol 3-biphosphate; PTI: PAMP-triggered immunity; qRT-PCR: quantitative reverse transcription PCR; SnRK2.6: SNF1-related protein kinase 2.6 in <i>A. thaliana</i>; TORC1: the rapamycin-sensitive Tor complex1; TRAF: tumor necrosis factor receptor-associated factor; WT: wild type plant; Yc: C-terminal fragment of YFP; YFP: yellow fluorescent protein; Yn: N-terminal fragment of YFP.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Bao</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University , Wuhan, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shao</LastName><ForeName>Lu</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University , Wuhan, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Jiali</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University , Wuhan, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Yan</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Ecology College, Lishui University , Lishui, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Guo</LastName><ForeName>Xiaoshuang</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University , Wuhan, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Peng</LastName><ForeName>Yujiao</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University , Wuhan, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cao</LastName><ForeName>Yangrong</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University , Wuhan, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lai</LastName><ForeName>Zhibing</ForeName><Initials>Z</Initials><AffiliationInfo><Affiliation>National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University , Wuhan, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>08</Month><Day>26</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Autophagy</MedlineTA><NlmUniqueID>101265188</NlmUniqueID><ISSNLinking>1554-8627</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N"> A. thaliana </Keyword><Keyword MajorTopicYN="N"> B. cinerea </Keyword><Keyword MajorTopicYN="N">ATG18a</Keyword><Keyword MajorTopicYN="N">BAK1</Keyword><Keyword MajorTopicYN="N">autophagy</Keyword><Keyword MajorTopicYN="N">resistance</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>8</Month><Day>18</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>8</Month><Day>18</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>8</Month><Day>18</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32804012</ArticleId><ArticleId IdType="doi">10.1080/15548627.2020.1810426</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>République populaire de Chine</li></country><region><li>Hubei</li></region><settlement><li>Wuhan</li></settlement></list><tree><country name="République populaire de Chine"><region name="Hubei"><name sortKey="Zhang, Bao" sort="Zhang, Bao" uniqKey="Zhang B" first="Bao" last="Zhang">Bao Zhang</name></region><name sortKey="Cao, Yangrong" sort="Cao, Yangrong" uniqKey="Cao Y" first="Yangrong" last="Cao">Yangrong Cao</name><name sortKey="Guo, Xiaoshuang" sort="Guo, Xiaoshuang" uniqKey="Guo X" first="Xiaoshuang" last="Guo">Xiaoshuang Guo</name><name sortKey="Lai, Zhibing" sort="Lai, Zhibing" uniqKey="Lai Z" first="Zhibing" last="Lai">Zhibing Lai</name><name sortKey="Peng, Yujiao" sort="Peng, Yujiao" uniqKey="Peng Y" first="Yujiao" last="Peng">Yujiao Peng</name><name sortKey="Shao, Lu" sort="Shao, Lu" uniqKey="Shao L" first="Lu" last="Shao">Lu Shao</name><name sortKey="Wang, Jiali" sort="Wang, Jiali" uniqKey="Wang J" first="Jiali" last="Wang">Jiali Wang</name><name sortKey="Zhang, Yan" sort="Zhang, Yan" uniqKey="Zhang Y" first="Yan" last="Zhang">Yan Zhang</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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