The rice NLR pair Pikp-1/Pikp-2 initiates cell death through receptor cooperation rather than negative regulation.
Identifieur interne : 000022 ( Main/Exploration ); précédent : 000021; suivant : 000023The rice NLR pair Pikp-1/Pikp-2 initiates cell death through receptor cooperation rather than negative regulation.
Auteurs : Rafał Zdrzałek [Royaume-Uni] ; Sophien Kamoun [Royaume-Uni] ; Ryohei Terauchi [Japon] ; Hiromasa Saitoh [Japon] ; Mark J. Banfield [Royaume-Uni]Source :
- PloS one [ 1932-6203 ] ; 2020.
Descripteurs français
- KwdFr :
- Domaines protéiques (MeSH), Liaison aux protéines (MeSH), Mort cellulaire (MeSH), Motifs d'acides aminés (MeSH), Oryza (cytologie), Oryza (métabolisme), Protéines NLR (composition chimique), Protéines NLR (métabolisme), Protéines végétales (composition chimique), Protéines végétales (métabolisme), Séquence d'acides aminés (MeSH).
- MESH :
- composition chimique : Protéines NLR, Protéines végétales.
- cytologie : Oryza.
- métabolisme : Oryza, Protéines NLR, Protéines végétales.
- Domaines protéiques, Liaison aux protéines, Mort cellulaire, Motifs d'acides aminés, Séquence d'acides aminés.
English descriptors
- KwdEn :
- MESH :
- chemical , chemistry : NLR Proteins, Plant Proteins.
- chemical , metabolism : NLR Proteins, Plant Proteins.
- cytology : Oryza.
- metabolism : Oryza.
- Amino Acid Motifs, Amino Acid Sequence, Cell Death, Protein Binding, Protein Domains.
Abstract
Plant NLR immune receptors are multidomain proteins that can function as specialized sensor/helper pairs. Paired NLR immune receptors are generally thought to function via negative regulation, where one NLR represses the activity of the second and detection of pathogen effectors relieves this repression to initiate immunity. However, whether this mechanism is common to all NLR pairs is not known. Here, we show that the rice NLR pair Pikp-1/Pikp-2, which confers resistance to strains of the blast pathogen Magnaporthe oryzae (syn. Pyricularia oryzae) expressing the AVR-PikD effector, functions via receptor cooperation, with effector-triggered activation requiring both NLRs to trigger the immune response. To investigate the mechanism of Pikp-1/Pikp-2 activation, we expressed truncated variants of these proteins, and made mutations in previously identified NLR sequence motifs. We found that any domain truncation, in either Pikp-1 or Pikp-2, prevented cell death in the presence of AVR-PikD, revealing that all domains are required for activity. Further, expression of individual Pikp-1 or Pikp-2 domains did not result in cell death. Mutations in the conserved P-loop and MHD sequence motifs in both Pikp-1 and Pikp-2 prevented cell death activation, demonstrating that these motifs are required for the function of the two partner NLRs. Finally, we showed that Pikp-1 and Pikp-2 associate to form homo- and hetero-complexes in planta in the absence of AVR-PikD; on co-expression the effector binds to Pikp-1 generating a tri-partite complex. Taken together, we provide evidence that Pikp-1 and Pikp-2 form a fine-tuned system that is activated by AVR-PikD via receptor cooperation rather than negative regulation.
DOI: 10.1371/journal.pone.0238616
PubMed: 32931489
PubMed Central: PMC7491719
Affiliations:
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Banfield</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biological Chemistry, John Innes Centre, Norwich, United Kingdom.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Biological Chemistry, John Innes Centre, Norwich</wicri:regionArea><wicri:noRegion>Norwich</wicri:noRegion></affiliation></author></analytic><series><title level="j">PloS one</title><idno type="eISSN">1932-6203</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Amino Acid Motifs (MeSH)</term><term>Amino Acid Sequence (MeSH)</term><term>Cell Death (MeSH)</term><term>NLR Proteins (chemistry)</term><term>NLR Proteins (metabolism)</term><term>Oryza (cytology)</term><term>Oryza (metabolism)</term><term>Plant Proteins (chemistry)</term><term>Plant Proteins (metabolism)</term><term>Protein Binding (MeSH)</term><term>Protein Domains (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Domaines protéiques (MeSH)</term><term>Liaison aux protéines (MeSH)</term><term>Mort cellulaire (MeSH)</term><term>Motifs d'acides aminés (MeSH)</term><term>Oryza (cytologie)</term><term>Oryza (métabolisme)</term><term>Protéines NLR (composition chimique)</term><term>Protéines NLR (métabolisme)</term><term>Protéines végétales (composition chimique)</term><term>Protéines végétales (métabolisme)</term><term>Séquence d'acides aminés (MeSH)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>NLR Proteins</term><term>Plant Proteins</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>NLR Proteins</term><term>Plant Proteins</term></keywords><keywords scheme="MESH" qualifier="composition chimique" xml:lang="fr"><term>Protéines NLR</term><term>Protéines végétales</term></keywords><keywords scheme="MESH" qualifier="cytologie" xml:lang="fr"><term>Oryza</term></keywords><keywords scheme="MESH" qualifier="cytology" xml:lang="en"><term>Oryza</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Oryza</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Oryza</term><term>Protéines NLR</term><term>Protéines végétales</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Amino Acid Motifs</term><term>Amino Acid Sequence</term><term>Cell Death</term><term>Protein Binding</term><term>Protein Domains</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Domaines protéiques</term><term>Liaison aux protéines</term><term>Mort cellulaire</term><term>Motifs d'acides aminés</term><term>Séquence d'acides aminés</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Plant NLR immune receptors are multidomain proteins that can function as specialized sensor/helper pairs. Paired NLR immune receptors are generally thought to function via negative regulation, where one NLR represses the activity of the second and detection of pathogen effectors relieves this repression to initiate immunity. However, whether this mechanism is common to all NLR pairs is not known. Here, we show that the rice NLR pair Pikp-1/Pikp-2, which confers resistance to strains of the blast pathogen Magnaporthe oryzae (syn. Pyricularia oryzae) expressing the AVR-PikD effector, functions via receptor cooperation, with effector-triggered activation requiring both NLRs to trigger the immune response. To investigate the mechanism of Pikp-1/Pikp-2 activation, we expressed truncated variants of these proteins, and made mutations in previously identified NLR sequence motifs. We found that any domain truncation, in either Pikp-1 or Pikp-2, prevented cell death in the presence of AVR-PikD, revealing that all domains are required for activity. Further, expression of individual Pikp-1 or Pikp-2 domains did not result in cell death. Mutations in the conserved P-loop and MHD sequence motifs in both Pikp-1 and Pikp-2 prevented cell death activation, demonstrating that these motifs are required for the function of the two partner NLRs. Finally, we showed that Pikp-1 and Pikp-2 associate to form homo- and hetero-complexes in planta in the absence of AVR-PikD; on co-expression the effector binds to Pikp-1 generating a tri-partite complex. Taken together, we provide evidence that Pikp-1 and Pikp-2 form a fine-tuned system that is activated by AVR-PikD via receptor cooperation rather than negative regulation.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">32931489</PMID><DateCompleted><Year>2020</Year><Month>10</Month><Day>28</Day></DateCompleted><DateRevised><Year>2020</Year><Month>10</Month><Day>28</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">1932-6203</ISSN><JournalIssue CitedMedium="Internet"><Volume>15</Volume><Issue>9</Issue><PubDate><Year>2020</Year></PubDate></JournalIssue><Title>PloS one</Title><ISOAbbreviation>PLoS One</ISOAbbreviation></Journal><ArticleTitle>The rice NLR pair Pikp-1/Pikp-2 initiates cell death through receptor cooperation rather than negative regulation.</ArticleTitle><Pagination><MedlinePgn>e0238616</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.pone.0238616</ELocationID><Abstract><AbstractText>Plant NLR immune receptors are multidomain proteins that can function as specialized sensor/helper pairs. Paired NLR immune receptors are generally thought to function via negative regulation, where one NLR represses the activity of the second and detection of pathogen effectors relieves this repression to initiate immunity. However, whether this mechanism is common to all NLR pairs is not known. Here, we show that the rice NLR pair Pikp-1/Pikp-2, which confers resistance to strains of the blast pathogen Magnaporthe oryzae (syn. Pyricularia oryzae) expressing the AVR-PikD effector, functions via receptor cooperation, with effector-triggered activation requiring both NLRs to trigger the immune response. To investigate the mechanism of Pikp-1/Pikp-2 activation, we expressed truncated variants of these proteins, and made mutations in previously identified NLR sequence motifs. We found that any domain truncation, in either Pikp-1 or Pikp-2, prevented cell death in the presence of AVR-PikD, revealing that all domains are required for activity. Further, expression of individual Pikp-1 or Pikp-2 domains did not result in cell death. Mutations in the conserved P-loop and MHD sequence motifs in both Pikp-1 and Pikp-2 prevented cell death activation, demonstrating that these motifs are required for the function of the two partner NLRs. Finally, we showed that Pikp-1 and Pikp-2 associate to form homo- and hetero-complexes in planta in the absence of AVR-PikD; on co-expression the effector binds to Pikp-1 generating a tri-partite complex. Taken together, we provide evidence that Pikp-1 and Pikp-2 form a fine-tuned system that is activated by AVR-PikD via receptor cooperation rather than negative regulation.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Zdrzałek</LastName><ForeName>Rafał</ForeName><Initials>R</Initials><Identifier Source="ORCID">0000-0003-3669-924X</Identifier><AffiliationInfo><Affiliation>Department of Biological Chemistry, John Innes Centre, Norwich, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kamoun</LastName><ForeName>Sophien</ForeName><Initials>S</Initials><Identifier Source="ORCID">0000-0002-0290-0315</Identifier><AffiliationInfo><Affiliation>The Sainsbury Laboratory, University of East Anglia, Norwich, United Kingdom.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Terauchi</LastName><ForeName>Ryohei</ForeName><Initials>R</Initials><Identifier Source="ORCID">0000-0002-0095-4651</Identifier><AffiliationInfo><Affiliation>Division of Genomics and Breeding, Iwate Biotechnology Research Centre, Iwate, Japan.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Laboratory of Crop Evolution, Graduate School of Agriculture, Kyoto University, Kyoto, Japan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Saitoh</LastName><ForeName>Hiromasa</ForeName><Initials>H</Initials><Identifier Source="ORCID">0000-0002-0124-9276</Identifier><AffiliationInfo><Affiliation>Laboratory of Plant Symbiotic and Parasitic Microbes, Department of Molecular Microbiology, Faculty of Life Sciences, Tokyo University of Agriculture, Tokyo, Japan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Banfield</LastName><ForeName>Mark J</ForeName><Initials>MJ</Initials><Identifier Source="ORCID">0000-0001-8921-3835</Identifier><AffiliationInfo><Affiliation>Department of Biological Chemistry, John Innes Centre, Norwich, United Kingdom.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>BB/M011216/1</GrantID><Acronym>BB_</Acronym><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant><Grant><GrantID>BB/P012574</GrantID><Acronym>BB_</Acronym><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant><Grant><GrantID>BB/M02198X </GrantID><Acronym>BB_</Acronym><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>09</Month><Day>15</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>PLoS One</MedlineTA><NlmUniqueID>101285081</NlmUniqueID><ISSNLinking>1932-6203</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D000070576">NLR Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D020816" MajorTopicYN="N">Amino Acid Motifs</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D000595" MajorTopicYN="N">Amino Acid Sequence</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D016923" MajorTopicYN="N">Cell Death</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D000070576" MajorTopicYN="N">NLR Proteins</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D012275" MajorTopicYN="N">Oryza</DescriptorName><QualifierName UI="Q000166" MajorTopicYN="Y">cytology</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName><QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D011485" MajorTopicYN="N">Protein Binding</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D000072417" MajorTopicYN="N">Protein Domains</DescriptorName></MeshHeading></MeshHeadingList><CoiStatement>The authors have declared that no competing interests exist.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate 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