A malectin-like receptor kinase regulates cell death and pattern-triggered immunity in soybean.
Identifieur interne : 000231 ( Main/Exploration ); précédent : 000230; suivant : 000232A malectin-like receptor kinase regulates cell death and pattern-triggered immunity in soybean.
Auteurs : Dongmei Wang [République populaire de Chine] ; Xiangxiu Liang [République populaire de Chine] ; Yazhou Bao [République populaire de Chine] ; Suxin Yang [République populaire de Chine] ; Xiong Zhang [République populaire de Chine] ; Hui Yu [République populaire de Chine] ; Qian Zhang [République populaire de Chine] ; Guangyuan Xu [République populaire de Chine] ; Xianzhong Feng [République populaire de Chine] ; Daolong Dou [République populaire de Chine]Source :
- EMBO reports [ 1469-3178 ] ; 2020.
Abstract
Plant cells can sense conserved molecular patterns through pattern recognition receptors (PRRs) and initiate pattern-triggered immunity (PTI). Details of the PTI signaling network are starting to be uncovered in Arabidopsis, but are still poorly understood in other species, including soybean (Glycine max). In this study, we perform a forward genetic screen for autoimmunity-related lesion mimic mutants (lmms) in soybean and identify two allelic mutants, which carry mutations in Glyma.13G054400, encoding a malectin-like receptor kinase (RK). The mutants exhibit enhanced resistance to both bacterial and oomycete pathogens, as well as elevated ROS production upon treatment with the bacterial pattern flg22. Overexpression of GmLMM1 gene in Nicotiana benthamiana severely suppresses flg22-triggered ROS production and oomycete pattern XEG1-induced cell death. We further show that GmLMM1 interacts with the flg22 receptor FLS2 and its co-receptor BAK1 to negatively regulate flg22-induced complex formation between them. Our study identifies an important component in PTI regulation and reveals that GmLMM1 acts as a molecular switch to control an appropriate immune activation, which may also be adapted to other PRR-mediated immune signaling in soybean.
DOI: 10.15252/embr.202050442
PubMed: 32924279
PubMed Central: PMC7645207
Affiliations:
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sort="Zhang, Qian" uniqKey="Zhang Q" first="Qian" last="Zhang">Qian Zhang</name><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Xu, Guangyuan" sort="Xu, Guangyuan" uniqKey="Xu G" first="Guangyuan" last="Xu">Guangyuan Xu</name><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de 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Wang</name><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory of Soybean Molecular Design Breeding, Northeast Institute of Geography and Agroecology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Changchun, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Soybean Molecular Design Breeding, Northeast Institute of Geography and Agroecology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Changchun</wicri:regionArea><placeName><settlement type="city">Changchun</settlement><region type="province">Jilin</region><region type="groupement">Dongbei</region></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>University of Chinese Academy of Sciences, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>University of Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Liang, Xiangxiu" sort="Liang, Xiangxiu" uniqKey="Liang X" first="Xiangxiu" last="Liang">Xiangxiu Liang</name><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Bao, Yazhou" sort="Bao, Yazhou" uniqKey="Bao Y" first="Yazhou" last="Bao">Yazhou Bao</name><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Yang, Suxin" sort="Yang, Suxin" uniqKey="Yang S" first="Suxin" last="Yang">Suxin Yang</name><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory of Soybean Molecular Design Breeding, Northeast Institute of Geography and Agroecology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Changchun, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Soybean Molecular Design Breeding, Northeast Institute of Geography and Agroecology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Changchun</wicri:regionArea><placeName><settlement type="city">Changchun</settlement><region type="province">Jilin</region><region type="groupement">Dongbei</region></placeName></affiliation></author><author><name sortKey="Zhang, Xiong" sort="Zhang, Xiong" uniqKey="Zhang X" first="Xiong" last="Zhang">Xiong Zhang</name><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Yu, Hui" sort="Yu, Hui" uniqKey="Yu H" first="Hui" last="Yu">Hui Yu</name><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory of Soybean Molecular Design Breeding, Northeast Institute of Geography and Agroecology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Changchun, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Soybean Molecular Design Breeding, Northeast Institute of Geography and Agroecology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Changchun</wicri:regionArea><placeName><settlement type="city">Changchun</settlement><region type="province">Jilin</region><region type="groupement">Dongbei</region></placeName></affiliation></author><author><name sortKey="Zhang, Qian" sort="Zhang, Qian" uniqKey="Zhang Q" first="Qian" last="Zhang">Qian Zhang</name><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Xu, Guangyuan" sort="Xu, Guangyuan" uniqKey="Xu G" first="Guangyuan" last="Xu">Guangyuan Xu</name><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Feng, Xianzhong" sort="Feng, Xianzhong" uniqKey="Feng X" first="Xianzhong" last="Feng">Xianzhong Feng</name><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory of Soybean Molecular Design Breeding, Northeast Institute of Geography and Agroecology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Changchun, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Soybean Molecular Design Breeding, Northeast Institute of Geography and Agroecology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Changchun</wicri:regionArea><placeName><settlement type="city">Changchun</settlement><region type="province">Jilin</region><region type="groupement">Dongbei</region></placeName></affiliation></author><author><name sortKey="Dou, Daolong" sort="Dou, Daolong" uniqKey="Dou D" first="Daolong" last="Dou">Daolong Dou</name><affiliation wicri:level="3"><nlm:affiliation>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>College of Plant Protection, Nanjing Agricultural University, Nanjing</wicri:regionArea><wicri:noRegion>Nanjing</wicri:noRegion></affiliation></author></analytic><series><title level="j">EMBO reports</title><idno type="eISSN">1469-3178</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 cells can sense conserved molecular patterns through pattern recognition receptors (PRRs) and initiate pattern-triggered immunity (PTI). Details of the PTI signaling network are starting to be uncovered in Arabidopsis, but are still poorly understood in other species, including soybean (Glycine max). In this study, we perform a forward genetic screen for autoimmunity-related lesion mimic mutants (lmms) in soybean and identify two allelic mutants, which carry mutations in Glyma.13G054400, encoding a malectin-like receptor kinase (RK). The mutants exhibit enhanced resistance to both bacterial and oomycete pathogens, as well as elevated ROS production upon treatment with the bacterial pattern flg22. Overexpression of GmLMM1 gene in Nicotiana benthamiana severely suppresses flg22-triggered ROS production and oomycete pattern XEG1-induced cell death. We further show that GmLMM1 interacts with the flg22 receptor FLS2 and its co-receptor BAK1 to negatively regulate flg22-induced complex formation between them. Our study identifies an important component in PTI regulation and reveals that GmLMM1 acts as a molecular switch to control an appropriate immune activation, which may also be adapted to other PRR-mediated immune signaling in soybean.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">32924279</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>14</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1469-3178</ISSN><JournalIssue CitedMedium="Internet"><Volume>21</Volume><Issue>11</Issue><PubDate><Year>2020</Year><Month>Nov</Month><Day>05</Day></PubDate></JournalIssue><Title>EMBO reports</Title><ISOAbbreviation>EMBO Rep</ISOAbbreviation></Journal><ArticleTitle>A malectin-like receptor kinase regulates cell death and pattern-triggered immunity in soybean.</ArticleTitle><Pagination><MedlinePgn>e50442</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.15252/embr.202050442</ELocationID><Abstract><AbstractText>Plant cells can sense conserved molecular patterns through pattern recognition receptors (PRRs) and initiate pattern-triggered immunity (PTI). Details of the PTI signaling network are starting to be uncovered in Arabidopsis, but are still poorly understood in other species, including soybean (Glycine max). In this study, we perform a forward genetic screen for autoimmunity-related lesion mimic mutants (lmms) in soybean and identify two allelic mutants, which carry mutations in Glyma.13G054400, encoding a malectin-like receptor kinase (RK). The mutants exhibit enhanced resistance to both bacterial and oomycete pathogens, as well as elevated ROS production upon treatment with the bacterial pattern flg22. Overexpression of GmLMM1 gene in Nicotiana benthamiana severely suppresses flg22-triggered ROS production and oomycete pattern XEG1-induced cell death. We further show that GmLMM1 interacts with the flg22 receptor FLS2 and its co-receptor BAK1 to negatively regulate flg22-induced complex formation between them. Our study identifies an important component in PTI regulation and reveals that GmLMM1 acts as a molecular switch to control an appropriate immune activation, which may also be adapted to other PRR-mediated immune signaling in soybean.</AbstractText><CopyrightInformation>© 2020 The Authors. Published under the terms of the CC BY 4.0 license.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y" EqualContrib="Y"><LastName>Wang</LastName><ForeName>Dongmei</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Key Laboratory of Soybean Molecular Design Breeding, Northeast Institute of Geography and Agroecology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Changchun, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>University of Chinese Academy of Sciences, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y" EqualContrib="Y"><LastName>Liang</LastName><ForeName>Xiangxiu</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bao</LastName><ForeName>Yazhou</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yang</LastName><ForeName>Suxin</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Key Laboratory of Soybean Molecular Design Breeding, Northeast Institute of Geography and Agroecology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Changchun, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Xiong</ForeName><Initials>X</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-2044-6929</Identifier><AffiliationInfo><Affiliation>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yu</LastName><ForeName>Hui</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Key Laboratory of Soybean Molecular Design Breeding, Northeast Institute of Geography and Agroecology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Changchun, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Qian</ForeName><Initials>Q</Initials><AffiliationInfo><Affiliation>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xu</LastName><ForeName>Guangyuan</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Feng</LastName><ForeName>Xianzhong</ForeName><Initials>X</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-7129-3731</Identifier><AffiliationInfo><Affiliation>Key Laboratory of Soybean Molecular Design Breeding, Northeast Institute of Geography and Agroecology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Changchun, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dou</LastName><ForeName>Daolong</ForeName><Initials>D</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-5226-6642</Identifier><AffiliationInfo><Affiliation>Key Laboratory of Pest Monitoring and Green Management, MOA and College of Plant Protection, China Agricultural University, Beijing, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>College of Plant Protection, Nanjing Agricultural University, Nanjing, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>2016YFD0101900</GrantID><Agency>MOST|National Key Research and Development Program of China</Agency><Country></Country></Grant><Grant><GrantID>31625023</GrantID><Agency>National Natural Science Foundation of China (NSF)</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>09</Month><Day>14</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>EMBO Rep</MedlineTA><NlmUniqueID>100963049</NlmUniqueID><ISSNLinking>1469-221X</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Glycine max
</Keyword><Keyword MajorTopicYN="N">cell death</Keyword><Keyword MajorTopicYN="N">lesion mimic mutant</Keyword><Keyword MajorTopicYN="N">malectin-like receptor kinase</Keyword><Keyword MajorTopicYN="N">pattern-triggered immunity</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>03</Month><Day>16</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>08</Month><Day>02</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>08</Month><Day>10</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>9</Month><Day>15</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>9</Month><Day>15</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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