Dissection of Cell Death Induction by Wheat Stem Rust Resistance Protein Sr35 and Its Matching Effector AvrSr35.
Identifieur interne : 000019 ( Main/Exploration ); précédent : 000018; suivant : 000020Dissection of Cell Death Induction by Wheat Stem Rust Resistance Protein Sr35 and Its Matching Effector AvrSr35.
Auteurs : Stephen Bolus [États-Unis] ; Eduard Akhunov [États-Unis] ; Gitta Coaker ; Jorge Dubcovsky [États-Unis]Source :
- Molecular plant-microbe interactions : MPMI [ 0894-0282 ] ; 2020.
Descripteurs français
- KwdFr :
- MESH :
- génétique : Mort cellulaire, Protéines végétales, Résistance à la maladie, Triticum.
- microbiologie : Triticum.
English descriptors
- KwdEn :
- MESH :
- chemical , genetics : Plant Proteins.
- genetics : Cell Death, Disease Resistance, Triticum.
- microbiology : Triticum.
Abstract
Nucleotide-binding leucine-rich repeat receptors (NLRs) are the most abundant type of immune receptors in plants and can trigger a rapid cell-death (hypersensitive) response upon sensing pathogens. We previously cloned the wheat NLR Sr35, which encodes a coiled-coil (CC) NLR that confers resistance to the virulent wheat stem rust race Ug99. Here, we investigated Sr35 signaling after Agrobacterium-mediated transient expression in Nicotiana benthamiana. Expression of Sr35 in N. benthamiana leaves triggered a mild cell-death response, which is enhanced in the autoactive mutant Sr35 D503V. The N-terminal tagging of Sr35 with green fluorescent protein (GFP) blocked the induction of cell death, whereas a C-terminal GFP tag did not. No domain truncations of Sr35 generated cell-death responses as strong as the wild type, but a truncation including the NB-ARC (nucleotide binding adaptor) shared by APAF-1, R proteins, and CED-4 domains in combination with the D503V autoactive mutation triggered cell death. In addition, coexpression of Sr35 with the matching pathogen effector protein AvrSr35 resulted in robust cell death and electrolyte leakage levels that were similar to autoactive Sr35 and significantly higher than Sr35 alone. Coexpression of Sr35-CC-NB-ARC and AvrSr35 did not induce cell death, confirming the importance of the leucine-rich repeat (LRR) domain for AvrSr35 recognition. These findings were confirmed through Agrobacterium-mediated transient expression in barley. Taken together, these results implicate the CC-NB-ARC domains of Sr35 in inducing cell death and the LRR domain in AvrSr35 recognition.[Formula: see text] Copyright © 2020 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.
DOI: 10.1094/MPMI-08-19-0216-R
PubMed: 31556346
PubMed Central: PMC7309591
Affiliations:
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California, Davis.</nlm:affiliation><wicri:noCountry code="subField">Davis</wicri:noCountry></affiliation></author><author><name sortKey="Akhunov, Eduard" sort="Akhunov, Eduard" uniqKey="Akhunov E" first="Eduard" last="Akhunov">Eduard Akhunov</name><affiliation wicri:level="2"><nlm:affiliation>Department of Plant Pathology, Kansas State University, Manhattan, KS 66506, U.S.A.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Pathology, Kansas State University, Manhattan, KS 66506</wicri:regionArea><placeName><region type="state">Kansas</region></placeName></affiliation></author><author><name sortKey="Coaker, Gitta" sort="Coaker, Gitta" uniqKey="Coaker G" first="Gitta" last="Coaker">Gitta Coaker</name><affiliation><nlm:affiliation>Department of Plant Pathology, University of California, Davis.</nlm:affiliation><wicri:noCountry code="subField">Davis</wicri:noCountry></affiliation></author><author><name sortKey="Dubcovsky, Jorge" sort="Dubcovsky, Jorge" uniqKey="Dubcovsky J" first="Jorge" last="Dubcovsky">Jorge Dubcovsky</name><affiliation wicri:level="2"><nlm:affiliation>Department of Plant Sciences, University of California, Davis, CA 95616, U.S.A.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Sciences, University of California, Davis, CA 95616</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Howard Hughes Medical Institute, Chevy Chase, MD 20815, U.S.A.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Howard Hughes Medical Institute, Chevy Chase, MD 20815</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author></analytic><series><title level="j">Molecular plant-microbe interactions : MPMI</title><idno type="ISSN">0894-0282</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Cell Death (genetics)</term><term>Disease Resistance (genetics)</term><term>Plant Proteins (genetics)</term><term>Triticum (genetics)</term><term>Triticum (microbiology)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Mort cellulaire (génétique)</term><term>Protéines végétales (génétique)</term><term>Résistance à la maladie (génétique)</term><term>Triticum (génétique)</term><term>Triticum (microbiologie)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Plant Proteins</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Cell Death</term><term>Disease Resistance</term><term>Triticum</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Mort cellulaire</term><term>Protéines végétales</term><term>Résistance à la maladie</term><term>Triticum</term></keywords><keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr"><term>Triticum</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Triticum</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Nucleotide-binding leucine-rich repeat receptors (NLRs) are the most abundant type of immune receptors in plants and can trigger a rapid cell-death (hypersensitive) response upon sensing pathogens. We previously cloned the wheat NLR <i>Sr35</i>, which encodes a coiled-coil (CC) NLR that confers resistance to the virulent wheat stem rust race Ug99. Here, we investigated Sr35 signaling after <i>Agrobacterium</i><i>-</i>mediated transient expression in <i>Nicotiana benthamiana.</i> Expression of Sr35 in <i>N. benthamiana</i> leaves triggered a mild cell-death response, which is enhanced in the autoactive mutant Sr35 D503V. The N-terminal tagging of Sr35 with green fluorescent protein (GFP) blocked the induction of cell death, whereas a C-terminal GFP tag did not. No domain truncations of Sr35 generated cell-death responses as strong as the wild type, but a truncation including the NB-ARC (nucleotide binding adaptor) shared by APAF-1, R proteins, and CED-4 domains in combination with the D503V autoactive mutation triggered cell death. In addition, coexpression of Sr35 with the matching pathogen effector protein AvrSr35 resulted in robust cell death and electrolyte leakage levels that were similar to autoactive Sr35 and significantly higher than Sr35 alone. Coexpression of Sr35-CC-NB-ARC and AvrSr35 did not induce cell death, confirming the importance of the leucine-rich repeat (LRR) domain for AvrSr35 recognition. These findings were confirmed through <i>Agrobacterium</i>-mediated transient expression in barley. Taken together, these results implicate the CC-NB-ARC domains of Sr35 in inducing cell death and the LRR domain in AvrSr35 recognition.[Formula: see text] Copyright © 2020 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" IndexingMethod="Curated" Owner="NLM"><PMID Version="1">31556346</PMID><DateCompleted><Year>2020</Year><Month>03</Month><Day>02</Day></DateCompleted><DateRevised><Year>2020</Year><Month>06</Month><Day>24</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Print">0894-0282</ISSN><JournalIssue CitedMedium="Print"><Volume>33</Volume><Issue>2</Issue><PubDate><Year>2020</Year><Month>Feb</Month></PubDate></JournalIssue><Title>Molecular plant-microbe interactions : MPMI</Title><ISOAbbreviation>Mol Plant Microbe Interact</ISOAbbreviation></Journal><ArticleTitle>Dissection of Cell Death Induction by Wheat Stem Rust Resistance Protein Sr35 and Its Matching Effector AvrSr35.</ArticleTitle><Pagination><MedlinePgn>308-319</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1094/MPMI-08-19-0216-R</ELocationID><Abstract><AbstractText>Nucleotide-binding leucine-rich repeat receptors (NLRs) are the most abundant type of immune receptors in plants and can trigger a rapid cell-death (hypersensitive) response upon sensing pathogens. We previously cloned the wheat NLR <i>Sr35</i>, which encodes a coiled-coil (CC) NLR that confers resistance to the virulent wheat stem rust race Ug99. Here, we investigated Sr35 signaling after <i>Agrobacterium</i><i>-</i>mediated transient expression in <i>Nicotiana benthamiana.</i> Expression of Sr35 in <i>N. benthamiana</i> leaves triggered a mild cell-death response, which is enhanced in the autoactive mutant Sr35 D503V. The N-terminal tagging of Sr35 with green fluorescent protein (GFP) blocked the induction of cell death, whereas a C-terminal GFP tag did not. No domain truncations of Sr35 generated cell-death responses as strong as the wild type, but a truncation including the NB-ARC (nucleotide binding adaptor) shared by APAF-1, R proteins, and CED-4 domains in combination with the D503V autoactive mutation triggered cell death. In addition, coexpression of Sr35 with the matching pathogen effector protein AvrSr35 resulted in robust cell death and electrolyte leakage levels that were similar to autoactive Sr35 and significantly higher than Sr35 alone. Coexpression of Sr35-CC-NB-ARC and AvrSr35 did not induce cell death, confirming the importance of the leucine-rich repeat (LRR) domain for AvrSr35 recognition. These findings were confirmed through <i>Agrobacterium</i>-mediated transient expression in barley. Taken together, these results implicate the CC-NB-ARC domains of Sr35 in inducing cell death and the LRR domain in AvrSr35 recognition.[Formula: see text] Copyright © 2020 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Bolus</LastName><ForeName>Stephen</ForeName><Initials>S</Initials><Identifier Source="ORCID">http://orcid.org/0000-0001-5472-095X</Identifier><AffiliationInfo><Affiliation>Department of Plant Sciences, University of California, Davis, CA 95616, U.S.A.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Plant Pathology, University of California, Davis.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Akhunov</LastName><ForeName>Eduard</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, Kansas State University, Manhattan, KS 66506, U.S.A.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Coaker</LastName><ForeName>Gitta</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology, University of California, Davis.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dubcovsky</LastName><ForeName>Jorge</ForeName><Initials>J</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-7571-4345</Identifier><AffiliationInfo><Affiliation>Department of Plant Sciences, University of California, Davis, CA 95616, U.S.A.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Howard Hughes Medical Institute, Chevy Chase, MD 20815, U.S.A.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>R01 GM092772</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>2019</Year><Month>12</Month><Day>16</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Mol Plant Microbe Interact</MedlineTA><NlmUniqueID>9107902</NlmUniqueID><ISSNLinking>0894-0282</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D016923" MajorTopicYN="Y">Cell Death</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D060467" MajorTopicYN="Y">Disease Resistance</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D014908" MajorTopicYN="Y">Triticum</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName></MeshHeading></MeshHeadingList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">AvrSr35</Keyword><Keyword MajorTopicYN="N">Puccinia graminis</Keyword><Keyword MajorTopicYN="N">Sr35</Keyword><Keyword MajorTopicYN="N">barley</Keyword><Keyword MajorTopicYN="N">cell death</Keyword><Keyword MajorTopicYN="N">disease resistance</Keyword><Keyword MajorTopicYN="N">effector</Keyword><Keyword MajorTopicYN="N">hypersensitive response</Keyword><Keyword MajorTopicYN="N">nucleotide-binding leucine-rich repeat receptor</Keyword><Keyword MajorTopicYN="N">stem rust</Keyword><Keyword MajorTopicYN="N">wheat</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>9</Month><Day>27</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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