Dynamic regulation of Pep-induced immunity through post-translational control of defence transcript splicing.
Identifieur interne : 000168 ( Main/Exploration ); précédent : 000167; suivant : 000169Dynamic regulation of Pep-induced immunity through post-translational control of defence transcript splicing.
Auteurs : Keini Dressano [États-Unis] ; Philipp R. Weckwerth [États-Unis] ; Elly Poretsky [États-Unis] ; Yohei Takahashi [États-Unis] ; Carleen Villarreal [États-Unis] ; Zhouxin Shen [États-Unis] ; Julian I. Schroeder [États-Unis] ; Steven P. Briggs [États-Unis] ; Alisa Huffaker [États-Unis]Source :
- Nature plants [ 2055-0278 ] ; 2020.
Abstract
The survival of all living organisms requires the ability to detect attacks and swiftly counter them with protective immune responses. Despite considerable mechanistic advances, the interconnectivity of signalling modules often remains unclear. A newly characterized protein, IMMUNOREGULATORY RNA-BINDING PROTEIN (IRR), negatively regulates immune responses in both maize and Arabidopsis, with disrupted function resulting in enhanced disease resistance. IRR associates with and promotes canonical splicing of transcripts encoding defence signalling proteins, including the key negative regulator of pattern-recognition receptor signalling complexes, CALCIUM-DEPENDENT PROTEIN KINASE 28 (CPK28). On immune activation by Plant Elicitor Peptides (Peps), IRR is dephosphorylated, disrupting interaction with CPK28 transcripts and resulting in the accumulation of an alternative splice variant encoding a truncated CPK28 protein with impaired kinase activity and diminished function as a negative regulator. We demonstrate a new mechanism linking Pep-induced post-translational modification of IRR with post-transcriptionally mediated attenuation of CPK28 function to dynamically amplify Pep signalling and immune output.
DOI: 10.1038/s41477-020-0724-1
PubMed: 32690890
PubMed Central: PMC7482133
Affiliations:
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Weckwerth</name><affiliation wicri:level="2"><nlm:affiliation>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Poretsky, Elly" sort="Poretsky, Elly" uniqKey="Poretsky E" first="Elly" last="Poretsky">Elly Poretsky</name><affiliation wicri:level="2"><nlm:affiliation>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Takahashi, Yohei" sort="Takahashi, Yohei" uniqKey="Takahashi Y" first="Yohei" last="Takahashi">Yohei Takahashi</name><affiliation wicri:level="2"><nlm:affiliation>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Villarreal, Carleen" sort="Villarreal, Carleen" uniqKey="Villarreal C" first="Carleen" last="Villarreal">Carleen Villarreal</name><affiliation wicri:level="2"><nlm:affiliation>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Shen, Zhouxin" sort="Shen, Zhouxin" uniqKey="Shen Z" first="Zhouxin" last="Shen">Zhouxin Shen</name><affiliation wicri:level="2"><nlm:affiliation>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Schroeder, Julian I" sort="Schroeder, Julian I" uniqKey="Schroeder J" first="Julian I" last="Schroeder">Julian I. Schroeder</name><affiliation wicri:level="2"><nlm:affiliation>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Briggs, Steven P" sort="Briggs, Steven P" uniqKey="Briggs S" first="Steven P" last="Briggs">Steven P. Briggs</name><affiliation wicri:level="2"><nlm:affiliation>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Huffaker, Alisa" sort="Huffaker, Alisa" uniqKey="Huffaker A" first="Alisa" last="Huffaker">Alisa Huffaker</name><affiliation wicri:level="2"><nlm:affiliation>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA, USA. ahuffaker@ucsd.edu.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author></analytic><series><title level="j">Nature plants</title><idno type="eISSN">2055-0278</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">The survival of all living organisms requires the ability to detect attacks and swiftly counter them with protective immune responses. Despite considerable mechanistic advances, the interconnectivity of signalling modules often remains unclear. A newly characterized protein, IMMUNOREGULATORY RNA-BINDING PROTEIN (IRR), negatively regulates immune responses in both maize and Arabidopsis, with disrupted function resulting in enhanced disease resistance. IRR associates with and promotes canonical splicing of transcripts encoding defence signalling proteins, including the key negative regulator of pattern-recognition receptor signalling complexes, CALCIUM-DEPENDENT PROTEIN KINASE 28 (CPK28). On immune activation by Plant Elicitor Peptides (Peps), IRR is dephosphorylated, disrupting interaction with CPK28 transcripts and resulting in the accumulation of an alternative splice variant encoding a truncated CPK28 protein with impaired kinase activity and diminished function as a negative regulator. We demonstrate a new mechanism linking Pep-induced post-translational modification of IRR with post-transcriptionally mediated attenuation of CPK28 function to dynamically amplify Pep signalling and immune output.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32690890</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>10</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">2055-0278</ISSN><JournalIssue CitedMedium="Internet"><Volume>6</Volume><Issue>8</Issue><PubDate><Year>2020</Year><Month>08</Month></PubDate></JournalIssue><Title>Nature plants</Title><ISOAbbreviation>Nat Plants</ISOAbbreviation></Journal><ArticleTitle>Dynamic regulation of Pep-induced immunity through post-translational control of defence transcript splicing.</ArticleTitle><Pagination><MedlinePgn>1008-1019</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1038/s41477-020-0724-1</ELocationID><Abstract><AbstractText>The survival of all living organisms requires the ability to detect attacks and swiftly counter them with protective immune responses. Despite considerable mechanistic advances, the interconnectivity of signalling modules often remains unclear. A newly characterized protein, IMMUNOREGULATORY RNA-BINDING PROTEIN (IRR), negatively regulates immune responses in both maize and Arabidopsis, with disrupted function resulting in enhanced disease resistance. IRR associates with and promotes canonical splicing of transcripts encoding defence signalling proteins, including the key negative regulator of pattern-recognition receptor signalling complexes, CALCIUM-DEPENDENT PROTEIN KINASE 28 (CPK28). On immune activation by Plant Elicitor Peptides (Peps), IRR is dephosphorylated, disrupting interaction with CPK28 transcripts and resulting in the accumulation of an alternative splice variant encoding a truncated CPK28 protein with impaired kinase activity and diminished function as a negative regulator. We demonstrate a new mechanism linking Pep-induced post-translational modification of IRR with post-transcriptionally mediated attenuation of CPK28 function to dynamically amplify Pep signalling and immune output.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Dressano</LastName><ForeName>Keini</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Weckwerth</LastName><ForeName>Philipp R</ForeName><Initials>PR</Initials><Identifier Source="ORCID">0000-0002-4464-7979</Identifier><AffiliationInfo><Affiliation>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Poretsky</LastName><ForeName>Elly</ForeName><Initials>E</Initials><Identifier Source="ORCID">0000-0002-6116-6827</Identifier><AffiliationInfo><Affiliation>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Takahashi</LastName><ForeName>Yohei</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Villarreal</LastName><ForeName>Carleen</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shen</LastName><ForeName>Zhouxin</ForeName><Initials>Z</Initials><Identifier Source="ORCID">0000-0002-7487-4064</Identifier><AffiliationInfo><Affiliation>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schroeder</LastName><ForeName>Julian I</ForeName><Initials>JI</Initials><Identifier Source="ORCID">0000-0002-3283-5972</Identifier><AffiliationInfo><Affiliation>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Briggs</LastName><ForeName>Steven P</ForeName><Initials>SP</Initials><AffiliationInfo><Affiliation>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Huffaker</LastName><ForeName>Alisa</ForeName><Initials>A</Initials><Identifier Source="ORCID">0000-0002-3886-8433</Identifier><AffiliationInfo><Affiliation>Section of Cell and Developmental Biology, UC San Diego, San Diego, CA, USA. ahuffaker@ucsd.edu.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>R01 GM060396</GrantID><Acronym>GM</Acronym><Agency>NIGMS NIH HHS</Agency><Country>United States</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>07</Month><Day>20</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Nat Plants</MedlineTA><NlmUniqueID>101651677</NlmUniqueID><ISSNLinking>2055-0278</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><CommentsCorrectionsList><CommentsCorrections RefType="CommentIn"><RefSource>Nat Plants. 2020 Aug;6(8):912-913</RefSource><PMID Version="1">32690889</PMID></CommentsCorrections></CommentsCorrectionsList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>08</Month><Day>01</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>06</Month><Day>11</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>7</Month><Day>22</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>7</Month><Day>22</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>7</Month><Day>22</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32690890</ArticleId><ArticleId IdType="doi">10.1038/s41477-020-0724-1</ArticleId><ArticleId IdType="pii">10.1038/s41477-020-0724-1</ArticleId><ArticleId IdType="pmc">PMC7482133</ArticleId><ArticleId IdType="mid">NIHMS1624141</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>États-Unis</li></country><region><li>Californie</li></region></list><tree><country name="États-Unis"><region name="Californie"><name sortKey="Dressano, Keini" sort="Dressano, Keini" uniqKey="Dressano K" first="Keini" last="Dressano">Keini Dressano</name></region><name sortKey="Briggs, Steven P" sort="Briggs, Steven P" uniqKey="Briggs S" first="Steven P" last="Briggs">Steven P. Briggs</name><name sortKey="Huffaker, Alisa" sort="Huffaker, Alisa" uniqKey="Huffaker A" first="Alisa" last="Huffaker">Alisa Huffaker</name><name sortKey="Poretsky, Elly" sort="Poretsky, Elly" uniqKey="Poretsky E" first="Elly" last="Poretsky">Elly Poretsky</name><name sortKey="Schroeder, Julian I" sort="Schroeder, Julian I" uniqKey="Schroeder J" first="Julian I" last="Schroeder">Julian I. Schroeder</name><name sortKey="Shen, Zhouxin" sort="Shen, Zhouxin" uniqKey="Shen Z" first="Zhouxin" last="Shen">Zhouxin Shen</name><name sortKey="Takahashi, Yohei" sort="Takahashi, Yohei" uniqKey="Takahashi Y" first="Yohei" last="Takahashi">Yohei Takahashi</name><name sortKey="Villarreal, Carleen" sort="Villarreal, Carleen" uniqKey="Villarreal C" first="Carleen" last="Villarreal">Carleen Villarreal</name><name sortKey="Weckwerth, Philipp R" sort="Weckwerth, Philipp R" uniqKey="Weckwerth P" first="Philipp R" last="Weckwerth">Philipp R. 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