Genome-wide functional analysis of hot pepper immune receptors reveals an autonomous NLR clade in seed plants.
Identifieur interne : 000150 ( Main/Exploration ); précédent : 000149; suivant : 000151Genome-wide functional analysis of hot pepper immune receptors reveals an autonomous NLR clade in seed plants.
Auteurs : Hye-Young Lee [Corée du Sud] ; Hyunggon Mang [Corée du Sud] ; Eunhye Choi [Corée du Sud] ; Ye-Eun Seo [Corée du Sud] ; Myung-Shin Kim [Corée du Sud] ; Soohyun Oh [Corée du Sud] ; Saet-Byul Kim [Corée du Sud] ; Doil Choi [Corée du Sud]Source :
- The New phytologist [ 1469-8137 ] ; 2020.
Abstract
Plants possess hundreds of intracellular immune receptors encoding nucleotide-binding domain leucine-rich repeat (NLR) proteins. Full-length NLRs or a specific domain of NLRs often induce plant cell death in the absence of pathogen infection. In this study we used genome-wide transient expression analysis to identify a group of NLRs (ANLs; ancient and autonomous NLRs) carrying autoactive coiled-coil (CCA ) domains in pepper (Capsicum annuum). CCA -mediated cell death mimics hypersensitive cell death triggered by the interaction between NLRs and pathogen effectors. Sequence alignment and mutagenesis analyses revealed that the intact α1 helix of CCA s is critical for both CCA - and ANL-mediated cell death. Cell death induced by CCA s does not require NRG1/ADR1 or NRC type helper NLRs, suggesting ANLs may function as singleton NLRs. We also found that CCA s localize to the plasma membrane, as demonstrated for Arabidopsis singleton NLR ZAR1. Extended studies revealed that autoactive CCA s are well conserved in other Solanaceae plants as well as in rice, a monocot plant. Further phylogenetic analyses revealed that ANLs are present in all tested seed plants (spermatophytes). Our study not only uncovers the autonomous NLR clade in plants but also provides powerful resources for dissecting the underlying molecular mechanism of NLR-mediated cell death in plants.
DOI: 10.1111/nph.16878
PubMed: 32810286
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Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul, 08826</wicri:regionArea><orgName type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation></author><author><name sortKey="Kim, Myung Shin" sort="Kim, Myung Shin" uniqKey="Kim M" first="Myung-Shin" last="Kim">Myung-Shin Kim</name><affiliation wicri:level="4"><nlm:affiliation>Plant Immunity Research Center, Seoul National University, Seoul, 08826, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Plant Immunity Research Center, Seoul National University, Seoul, 08826</wicri:regionArea><orgName type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation></author><author><name sortKey="Oh, Soohyun" sort="Oh, Soohyun" uniqKey="Oh S" first="Soohyun" last="Oh">Soohyun Oh</name><affiliation wicri:level="4"><nlm:affiliation>Plant Immunity Research Center, Seoul National University, Seoul, 08826, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Plant Immunity Research Center, Seoul National University, Seoul, 08826</wicri:regionArea><orgName type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation><affiliation wicri:level="4"><nlm:affiliation>Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul, 08826, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul, 08826</wicri:regionArea><orgName type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation></author><author><name sortKey="Kim, Saet Byul" sort="Kim, Saet Byul" uniqKey="Kim S" first="Saet-Byul" last="Kim">Saet-Byul Kim</name><affiliation wicri:level="4"><nlm:affiliation>Plant Immunity Research Center, Seoul National University, Seoul, 08826, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Plant Immunity Research Center, Seoul National University, Seoul, 08826</wicri:regionArea><orgName type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation></author><author><name sortKey="Choi, Doil" sort="Choi, Doil" uniqKey="Choi D" first="Doil" last="Choi">Doil Choi</name><affiliation wicri:level="4"><nlm:affiliation>Plant Immunity Research Center, Seoul National University, Seoul, 08826, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Plant Immunity Research Center, Seoul National University, Seoul, 08826</wicri:regionArea><orgName type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation><affiliation wicri:level="4"><nlm:affiliation>Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul, 08826, Korea.</nlm:affiliation><country xml:lang="fr">Corée du Sud</country><wicri:regionArea>Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul, 08826</wicri:regionArea><orgName type="university">Université nationale de Séoul</orgName><placeName><settlement type="city">Séoul</settlement></placeName></affiliation></author></analytic><series><title level="j">The New phytologist</title><idno type="eISSN">1469-8137</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">Plants possess hundreds of intracellular immune receptors encoding nucleotide-binding domain leucine-rich repeat (NLR) proteins. Full-length NLRs or a specific domain of NLRs often induce plant cell death in the absence of pathogen infection. In this study we used genome-wide transient expression analysis to identify a group of NLRs (ANLs; ancient and autonomous NLRs) carrying autoactive coiled-coil (CC<sup>A</sup> ) domains in pepper (Capsicum annuum). CC<sup>A</sup> -mediated cell death mimics hypersensitive cell death triggered by the interaction between NLRs and pathogen effectors. Sequence alignment and mutagenesis analyses revealed that the intact α1 helix of CC<sup>A</sup> s is critical for both CC<sup>A</sup> - and ANL-mediated cell death. Cell death induced by CC<sup>A</sup> s does not require NRG1/ADR1 or NRC type helper NLRs, suggesting ANLs may function as singleton NLRs. We also found that CC<sup>A</sup> s localize to the plasma membrane, as demonstrated for Arabidopsis singleton NLR ZAR1. Extended studies revealed that autoactive CC<sup>A</sup> s are well conserved in other Solanaceae plants as well as in rice, a monocot plant. Further phylogenetic analyses revealed that ANLs are present in all tested seed plants (spermatophytes). Our study not only uncovers the autonomous NLR clade in plants but also provides powerful resources for dissecting the underlying molecular mechanism of NLR-mediated cell death in plants.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">32810286</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>16</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1469-8137</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2020</Year><Month>Aug</Month><Day>18</Day></PubDate></JournalIssue><Title>The New phytologist</Title><ISOAbbreviation>New Phytol</ISOAbbreviation></Journal><ArticleTitle>Genome-wide functional analysis of hot pepper immune receptors reveals an autonomous NLR clade in seed plants.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1111/nph.16878</ELocationID><Abstract><AbstractText>Plants possess hundreds of intracellular immune receptors encoding nucleotide-binding domain leucine-rich repeat (NLR) proteins. Full-length NLRs or a specific domain of NLRs often induce plant cell death in the absence of pathogen infection. In this study we used genome-wide transient expression analysis to identify a group of NLRs (ANLs; ancient and autonomous NLRs) carrying autoactive coiled-coil (CC<sup>A</sup> ) domains in pepper (Capsicum annuum). CC<sup>A</sup> -mediated cell death mimics hypersensitive cell death triggered by the interaction between NLRs and pathogen effectors. Sequence alignment and mutagenesis analyses revealed that the intact α1 helix of CC<sup>A</sup> s is critical for both CC<sup>A</sup> - and ANL-mediated cell death. Cell death induced by CC<sup>A</sup> s does not require NRG1/ADR1 or NRC type helper NLRs, suggesting ANLs may function as singleton NLRs. We also found that CC<sup>A</sup> s localize to the plasma membrane, as demonstrated for Arabidopsis singleton NLR ZAR1. Extended studies revealed that autoactive CC<sup>A</sup> s are well conserved in other Solanaceae plants as well as in rice, a monocot plant. Further phylogenetic analyses revealed that ANLs are present in all tested seed plants (spermatophytes). Our study not only uncovers the autonomous NLR clade in plants but also provides powerful resources for dissecting the underlying molecular mechanism of NLR-mediated cell death in plants.</AbstractText><CopyrightInformation>© 2020 The Authors. New Phytologist © 2020 New Phytologist Trust.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Lee</LastName><ForeName>Hye-Young</ForeName><Initials>HY</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-3797-889X</Identifier><AffiliationInfo><Affiliation>Plant Immunity Research Center, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mang</LastName><ForeName>Hyunggon</ForeName><Initials>H</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-6366-1314</Identifier><AffiliationInfo><Affiliation>Plant Immunity Research Center, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Choi</LastName><ForeName>Eunhye</ForeName><Initials>E</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-2596-7229</Identifier><AffiliationInfo><Affiliation>Plant Immunity Research Center, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Seo</LastName><ForeName>Ye-Eun</ForeName><Initials>YE</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-6965-7658</Identifier><AffiliationInfo><Affiliation>Plant Immunity Research Center, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kim</LastName><ForeName>Myung-Shin</ForeName><Initials>MS</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-5967-4347</Identifier><AffiliationInfo><Affiliation>Plant Immunity Research Center, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Oh</LastName><ForeName>Soohyun</ForeName><Initials>S</Initials><Identifier Source="ORCID">https://orcid.org/0000-0003-0003-588X</Identifier><AffiliationInfo><Affiliation>Plant Immunity Research Center, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kim</LastName><ForeName>Saet-Byul</ForeName><Initials>SB</Initials><Identifier Source="ORCID">https://orcid.org/0000-0001-8826-6265</Identifier><AffiliationInfo><Affiliation>Plant Immunity Research Center, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Choi</LastName><ForeName>Doil</ForeName><Initials>D</Initials><Identifier Source="ORCID">https://orcid.org/0000-0002-4366-3627</Identifier><AffiliationInfo><Affiliation>Plant Immunity Research Center, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul, 08826, Korea.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>2018R1A5A1023599</GrantID><Agency>National Research Foundation</Agency><Country></Country></Grant><Grant><GrantID>2018R1A2A1A05019892</GrantID><Agency>National Research Foundation</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>08</Month><Day>18</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>New Phytol</MedlineTA><NlmUniqueID>9882884</NlmUniqueID><ISSNLinking>0028-646X</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Capsicum annuum
</Keyword><Keyword MajorTopicYN="N">cell death</Keyword><Keyword MajorTopicYN="N">coiled-coil domain</Keyword><Keyword MajorTopicYN="N">plant NLR</Keyword><Keyword MajorTopicYN="N">singleton NLR</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>04</Month><Day>16</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>08</Month><Day>07</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>8</Month><Day>19</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>8</Month><Day>19</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>8</Month><Day>19</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32810286</ArticleId><ArticleId IdType="doi">10.1111/nph.16878</ArticleId></ArticleIdList><ReferenceList><Title>References</Title><Reference><Citation>Adachi H, Contreras M, Harant A, Wu C, Derevnina L, Sakai T, Duggan C, Moratto E, Bozkurt TO, Maqbool A et al. 2019a. 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