PlantPathoEffV1, Main, Exploration, bibRecord, 000011

Two unequally redundant "helper" immune receptor families mediate Arabidopsis thaliana intracellular "sensor" immune receptor functions.

Identifieur interne : 000011 ( Main/Exploration ); précédent : 000010; suivant : 000012

Two unequally redundant "helper" immune receptor families mediate Arabidopsis thaliana intracellular "sensor" immune receptor functions.

Auteurs : Svenja C. Saile [Allemagne] ; Pierre Jacob [États-Unis] ; Baptiste Castel [Royaume-Uni] ; Lance M. Jubic [États-Unis] ; Isai Salas-Gonzáles [États-Unis] ; Marcel B Cker [Allemagne] ; Jonathan D G. Jones [Royaume-Uni] ; Jeffery L. Dangl [États-Unis] ; Farid El Kasmi [Allemagne]

Source :

PLoS biology [ 1545-7885 ] ; 2020.

RBID : pubmed:32925907

Descripteurs français

English descriptors

KwdEn :
- Arabidopsis (genetics), Arabidopsis (immunology), Arabidopsis Proteins (genetics), Arabidopsis Proteins (physiology), Disease Resistance (genetics), Disease Resistance (immunology), Gene Expression Regulation, Plant (MeSH), Intracellular Signaling Peptides and Proteins (genetics), Intracellular Signaling Peptides and Proteins (physiology), Multigene Family (genetics), Multigene Family (physiology), NLR Proteins (genetics), NLR Proteins (physiology), Plant Diseases (genetics), Plant Diseases (immunology), Plant Immunity (genetics), Plants, Genetically Modified (MeSH), Receptors, Immunologic (genetics), Receptors, Immunologic (physiology), Signal Transduction (genetics), Signal Transduction (immunology), Transcriptome (MeSH).
MESH :
- chemical , genetics : Arabidopsis Proteins, Intracellular Signaling Peptides and Proteins, NLR Proteins, Receptors, Immunologic.
- genetics : Arabidopsis, Disease Resistance, Multigene Family, Plant Diseases, Plant Immunity, Signal Transduction.
- immunology : Arabidopsis, Disease Resistance, Plant Diseases, Signal Transduction.
- chemical , physiology : Arabidopsis Proteins, Intracellular Signaling Peptides and Proteins, Multigene Family, NLR Proteins, Receptors, Immunologic.
- Gene Expression Regulation, Plant, Plants, Genetically Modified, Transcriptome.

Abstract

Plant nucleotide-binding (NB) leucine-rich repeat (LRR) receptor (NLR) proteins function as intracellular immune receptors that perceive the presence of pathogen-derived virulence proteins (effectors) to induce immune responses. The 2 major types of plant NLRs that "sense" pathogen effectors differ in their N-terminal domains: these are Toll/interleukin-1 receptor resistance (TIR) domain-containing NLRs (TNLs) and coiled-coil (CC) domain-containing NLRs (CNLs). In many angiosperms, the RESISTANCE TO POWDERY MILDEW 8 (RPW8)-CC domain containing NLR (RNL) subclass of CNLs is encoded by 2 gene families, ACTIVATED DISEASE RESISTANCE 1 (ADR1) and N REQUIREMENT GENE 1 (NRG1), that act as "helper" NLRs during multiple sensor NLR-mediated immune responses. Despite their important role in sensor NLR-mediated immunity, knowledge of the specific, redundant, and synergistic functions of helper RNLs is limited. We demonstrate that the ADR1 and NRG1 families act in an unequally redundant manner in basal resistance, effector-triggered immunity (ETI) and regulation of defense gene expression. We define RNL redundancy in ETI conferred by some TNLs and in basal resistance against virulent pathogens. We demonstrate that, in Arabidopsis thaliana, the 2 RNL families contribute specific functions in ETI initiated by specific CNLs and TNLs. Time-resolved whole genome expression profiling revealed that RNLs and "classical" CNLs trigger similar transcriptome changes, suggesting that RNLs act like other CNLs to mediate ETI downstream of sensor NLR activation. Together, our genetic data confirm that RNLs contribute to basal resistance, are fully required for TNL signaling, and can also support defense activation during CNL-mediated ETI.

DOI: 10.1371/journal.pbio.3000783
PubMed: 32925907
PubMed Central: PMC7514072

Affiliations:

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Le document en format XML

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<sourceDesc><biblStruct><analytic><title xml:lang="en">Two unequally redundant "helper" immune receptor families mediate Arabidopsis thaliana intracellular "sensor" immune receptor functions.</title>
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<orgName type="university">Université de Caroline du Nord à Chapel Hill</orgName>
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<affiliation wicri:level="4"><nlm:affiliation>Curriculum in Bioinformatics and Computational Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
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<placeName><region type="state">Caroline du Nord</region>
<settlement type="city">Chapel Hill (Caroline du Nord)</settlement>
</placeName>
<orgName type="university">Université de Caroline du Nord à Chapel Hill</orgName>
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<affiliation wicri:level="4"><nlm:affiliation>Carolina Center for Genome Sciences, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.</nlm:affiliation>
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</placeName>
<orgName type="university">Université de Caroline du Nord à Chapel Hill</orgName>
</affiliation>
<affiliation wicri:level="4"><nlm:affiliation>Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina</wicri:regionArea>
<placeName><region type="state">Caroline du Nord</region>
<settlement type="city">Chapel Hill (Caroline du Nord)</settlement>
</placeName>
<orgName type="university">Université de Caroline du Nord à Chapel Hill</orgName>
</affiliation>
</author>
<author><name sortKey="El Kasmi, Farid" sort="El Kasmi, Farid" uniqKey="El Kasmi F" first="Farid" last="El Kasmi">Farid El Kasmi</name>
<affiliation wicri:level="3"><nlm:affiliation>Center for Plant Molecular Biology, Eberhard Karls University of Tübingen, Tübingen, Germany.</nlm:affiliation>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Center for Plant Molecular Biology, Eberhard Karls University of Tübingen, Tübingen</wicri:regionArea>
<placeName><region type="land" nuts="1">Bade-Wurtemberg</region>
<region type="district" nuts="2">District de Tübingen</region>
<settlement type="city">Tübingen</settlement>
</placeName>
</affiliation>
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<series><title level="j">PLoS biology</title>
<idno type="eISSN">1545-7885</idno>
<imprint><date when="2020" type="published">2020</date>
</imprint>
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<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Arabidopsis (genetics)</term>
<term>Arabidopsis (immunology)</term>
<term>Arabidopsis Proteins (genetics)</term>
<term>Arabidopsis Proteins (physiology)</term>
<term>Disease Resistance (genetics)</term>
<term>Disease Resistance (immunology)</term>
<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Intracellular Signaling Peptides and Proteins (genetics)</term>
<term>Intracellular Signaling Peptides and Proteins (physiology)</term>
<term>Multigene Family (genetics)</term>
<term>Multigene Family (physiology)</term>
<term>NLR Proteins (genetics)</term>
<term>NLR Proteins (physiology)</term>
<term>Plant Diseases (genetics)</term>
<term>Plant Diseases (immunology)</term>
<term>Plant Immunity (genetics)</term>
<term>Plants, Genetically Modified (MeSH)</term>
<term>Receptors, Immunologic (genetics)</term>
<term>Receptors, Immunologic (physiology)</term>
<term>Signal Transduction (genetics)</term>
<term>Signal Transduction (immunology)</term>
<term>Transcriptome (MeSH)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>Arabidopsis (génétique)</term>
<term>Arabidopsis (immunologie)</term>
<term>Famille multigénique (génétique)</term>
<term>Famille multigénique (physiologie)</term>
<term>Immunité des plantes (génétique)</term>
<term>Maladies des plantes (génétique)</term>
<term>Maladies des plantes (immunologie)</term>
<term>Protéines NLR (génétique)</term>
<term>Protéines NLR (physiologie)</term>
<term>Protéines d'Arabidopsis (génétique)</term>
<term>Protéines d'Arabidopsis (physiologie)</term>
<term>Protéines et peptides de signalisation intracellulaire (génétique)</term>
<term>Protéines et peptides de signalisation intracellulaire (physiologie)</term>
<term>Récepteurs immunologiques (génétique)</term>
<term>Récepteurs immunologiques (physiologie)</term>
<term>Régulation de l'expression des gènes végétaux (MeSH)</term>
<term>Résistance à la maladie (génétique)</term>
<term>Résistance à la maladie (immunologie)</term>
<term>Transcriptome (MeSH)</term>
<term>Transduction du signal (génétique)</term>
<term>Transduction du signal (immunologie)</term>
<term>Végétaux génétiquement modifiés (MeSH)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Arabidopsis Proteins</term>
<term>Intracellular Signaling Peptides and Proteins</term>
<term>NLR Proteins</term>
<term>Receptors, Immunologic</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Arabidopsis</term>
<term>Disease Resistance</term>
<term>Multigene Family</term>
<term>Plant Diseases</term>
<term>Plant Immunity</term>
<term>Signal Transduction</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Arabidopsis</term>
<term>Famille multigénique</term>
<term>Immunité des plantes</term>
<term>Maladies des plantes</term>
<term>Protéines NLR</term>
<term>Protéines d'Arabidopsis</term>
<term>Protéines et peptides de signalisation intracellulaire</term>
<term>Récepteurs immunologiques</term>
<term>Résistance à la maladie</term>
<term>Transduction du signal</term>
</keywords>
<keywords scheme="MESH" qualifier="immunologie" xml:lang="fr"><term>Arabidopsis</term>
<term>Maladies des plantes</term>
<term>Résistance à la maladie</term>
<term>Transduction du signal</term>
</keywords>
<keywords scheme="MESH" qualifier="immunology" xml:lang="en"><term>Arabidopsis</term>
<term>Disease Resistance</term>
<term>Plant Diseases</term>
<term>Signal Transduction</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Famille multigénique</term>
<term>Protéines NLR</term>
<term>Protéines d'Arabidopsis</term>
<term>Protéines et peptides de signalisation intracellulaire</term>
<term>Récepteurs immunologiques</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="physiology" xml:lang="en"><term>Arabidopsis Proteins</term>
<term>Intracellular Signaling Peptides and Proteins</term>
<term>Multigene Family</term>
<term>NLR Proteins</term>
<term>Receptors, Immunologic</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Gene Expression Regulation, Plant</term>
<term>Plants, Genetically Modified</term>
<term>Transcriptome</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr"><term>Régulation de l'expression des gènes végétaux</term>
<term>Transcriptome</term>
<term>Végétaux génétiquement modifiés</term>
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<front><div type="abstract" xml:lang="en">Plant nucleotide-binding (NB) leucine-rich repeat (LRR) receptor (NLR) proteins function as intracellular immune receptors that perceive the presence of pathogen-derived virulence proteins (effectors) to induce immune responses. The 2 major types of plant NLRs that "sense" pathogen effectors differ in their N-terminal domains: these are Toll/interleukin-1 receptor resistance (TIR) domain-containing NLRs (TNLs) and coiled-coil (CC) domain-containing NLRs (CNLs). In many angiosperms, the RESISTANCE TO POWDERY MILDEW 8 (RPW8)-CC domain containing NLR (RNL) subclass of CNLs is encoded by 2 gene families, ACTIVATED DISEASE RESISTANCE 1 (ADR1) and N REQUIREMENT GENE 1 (NRG1), that act as "helper" NLRs during multiple sensor NLR-mediated immune responses. Despite their important role in sensor NLR-mediated immunity, knowledge of the specific, redundant, and synergistic functions of helper RNLs is limited. We demonstrate that the ADR1 and NRG1 families act in an unequally redundant manner in basal resistance, effector-triggered immunity (ETI) and regulation of defense gene expression. We define RNL redundancy in ETI conferred by some TNLs and in basal resistance against virulent pathogens. We demonstrate that, in Arabidopsis thaliana, the 2 RNL families contribute specific functions in ETI initiated by specific CNLs and TNLs. Time-resolved whole genome expression profiling revealed that RNLs and "classical" CNLs trigger similar transcriptome changes, suggesting that RNLs act like other CNLs to mediate ETI downstream of sensor NLR activation. Together, our genetic data confirm that RNLs contribute to basal resistance, are fully required for TNL signaling, and can also support defense activation during CNL-mediated ETI.</div>
</front>
</TEI>
<pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">32925907</PMID>
<DateCompleted><Year>2020</Year>
<Month>10</Month>
<Day>20</Day>
</DateCompleted>
<DateRevised><Year>2020</Year>
<Month>10</Month>
<Day>20</Day>
</DateRevised>
<Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">1545-7885</ISSN>
<JournalIssue CitedMedium="Internet"><Volume>18</Volume>
<Issue>9</Issue>
<PubDate><Year>2020</Year>
<Month>09</Month>
</PubDate>
</JournalIssue>
<Title>PLoS biology</Title>
<ISOAbbreviation>PLoS Biol</ISOAbbreviation>
</Journal>
<ArticleTitle>Two unequally redundant "helper" immune receptor families mediate Arabidopsis thaliana intracellular "sensor" immune receptor functions.</ArticleTitle>
<Pagination><MedlinePgn>e3000783</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.pbio.3000783</ELocationID>
<Abstract><AbstractText>Plant nucleotide-binding (NB) leucine-rich repeat (LRR) receptor (NLR) proteins function as intracellular immune receptors that perceive the presence of pathogen-derived virulence proteins (effectors) to induce immune responses. The 2 major types of plant NLRs that "sense" pathogen effectors differ in their N-terminal domains: these are Toll/interleukin-1 receptor resistance (TIR) domain-containing NLRs (TNLs) and coiled-coil (CC) domain-containing NLRs (CNLs). In many angiosperms, the RESISTANCE TO POWDERY MILDEW 8 (RPW8)-CC domain containing NLR (RNL) subclass of CNLs is encoded by 2 gene families, ACTIVATED DISEASE RESISTANCE 1 (ADR1) and N REQUIREMENT GENE 1 (NRG1), that act as "helper" NLRs during multiple sensor NLR-mediated immune responses. Despite their important role in sensor NLR-mediated immunity, knowledge of the specific, redundant, and synergistic functions of helper RNLs is limited. We demonstrate that the ADR1 and NRG1 families act in an unequally redundant manner in basal resistance, effector-triggered immunity (ETI) and regulation of defense gene expression. We define RNL redundancy in ETI conferred by some TNLs and in basal resistance against virulent pathogens. We demonstrate that, in Arabidopsis thaliana, the 2 RNL families contribute specific functions in ETI initiated by specific CNLs and TNLs. Time-resolved whole genome expression profiling revealed that RNLs and "classical" CNLs trigger similar transcriptome changes, suggesting that RNLs act like other CNLs to mediate ETI downstream of sensor NLR activation. Together, our genetic data confirm that RNLs contribute to basal resistance, are fully required for TNL signaling, and can also support defense activation during CNL-mediated ETI.</AbstractText>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Saile</LastName>
<ForeName>Svenja C</ForeName>
<Initials>SC</Initials>
<Identifier Source="ORCID">0000-0003-2258-3166</Identifier>
<AffiliationInfo><Affiliation>Center for Plant Molecular Biology, Eberhard Karls University of Tübingen, Tübingen, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Jacob</LastName>
<ForeName>Pierre</ForeName>
<Initials>P</Initials>
<Identifier Source="ORCID">0000-0002-1253-3256</Identifier>
<AffiliationInfo><Affiliation>Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Howard Hughes Medical Institute, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Castel</LastName>
<ForeName>Baptiste</ForeName>
<Initials>B</Initials>
<Identifier Source="ORCID">0000-0002-2722-0228</Identifier>
<AffiliationInfo><Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Jubic</LastName>
<ForeName>Lance M</ForeName>
<Initials>LM</Initials>
<AffiliationInfo><Affiliation>Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Howard Hughes Medical Institute, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Curriculum in Genetics and Molecular Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Salas-Gonzáles</LastName>
<ForeName>Isai</ForeName>
<Initials>I</Initials>
<AffiliationInfo><Affiliation>Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Howard Hughes Medical Institute, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Curriculum in Bioinformatics and Computational Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Bäcker</LastName>
<ForeName>Marcel</ForeName>
<Initials>M</Initials>
<Identifier Source="ORCID">0000-0003-2539-6243</Identifier>
<AffiliationInfo><Affiliation>Center for Plant Molecular Biology, Eberhard Karls University of Tübingen, Tübingen, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Jones</LastName>
<ForeName>Jonathan D G</ForeName>
<Initials>JDG</Initials>
<Identifier Source="ORCID">0000-0002-4953-261X</Identifier>
<AffiliationInfo><Affiliation>The Sainsbury Laboratory, Norwich Research Park, Norwich, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Dangl</LastName>
<ForeName>Jeffery L</ForeName>
<Initials>JL</Initials>
<Identifier Source="ORCID">0000-0003-3199-8654</Identifier>
<AffiliationInfo><Affiliation>Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Howard Hughes Medical Institute, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Curriculum in Genetics and Molecular Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Curriculum in Bioinformatics and Computational Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Carolina Center for Genome Sciences, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.</Affiliation>
</AffiliationInfo>
<AffiliationInfo><Affiliation>Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>El Kasmi</LastName>
<ForeName>Farid</ForeName>
<Initials>F</Initials>
<Identifier Source="ORCID">0000-0002-4634-7689</Identifier>
<AffiliationInfo><Affiliation>Center for Plant Molecular Biology, Eberhard Karls University of Tübingen, Tübingen, Germany.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<GrantList CompleteYN="Y"><Grant><Acronym>HHMI</Acronym>
<Agency>Howard Hughes Medical Institute</Agency>
<Country>United States</Country>
</Grant>
<Grant><GrantID>T32 GM007092</GrantID>
<Acronym>GM</Acronym>
<Agency>NIGMS NIH HHS</Agency>
<Country>United States</Country>
</Grant>
</GrantList>
<PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D052061">Research Support, N.I.H., Extramural</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
<PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType>
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<ArticleDate DateType="Electronic"><Year>2020</Year>
<Month>09</Month>
<Day>14</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo><Country>United States</Country>
<MedlineTA>PLoS Biol</MedlineTA>
<NlmUniqueID>101183755</NlmUniqueID>
<ISSNLinking>1544-9173</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList><Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="C479129">ADR1 protein, Arabidopsis</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="C000657425">AT5G66900 protein, Arabidopsis</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="C000657426">AT5G66910 protein, Arabidopsis</NameOfSubstance>
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<Chemical><RegistryNumber>0</RegistryNumber>
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<CitationSubset>IM</CitationSubset>
<MeshHeadingList><MeshHeading><DescriptorName UI="D017360" MajorTopicYN="N">Arabidopsis</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000276" MajorTopicYN="Y">immunology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D029681" MajorTopicYN="N">Arabidopsis Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D060467" MajorTopicYN="N">Disease Resistance</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D047908" MajorTopicYN="N">Intracellular Signaling Peptides and Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D005810" MajorTopicYN="N">Multigene Family</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D000070576" MajorTopicYN="N">NLR Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D057865" MajorTopicYN="N">Plant Immunity</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D030821" MajorTopicYN="N">Plants, Genetically Modified</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D011971" MajorTopicYN="N">Receptors, Immunologic</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D015398" MajorTopicYN="N">Signal Transduction</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D059467" MajorTopicYN="N">Transcriptome</DescriptorName>
</MeshHeading>
</MeshHeadingList>
<CoiStatement>The authors have declared that no competing interests exist.</CoiStatement>
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<Month>08</Month>
<Day>17</Day>
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<Month>09</Month>
<Day>24</Day>
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Two unequally redundant "helper" immune receptor families mediate Arabidopsis thaliana intracellular "sensor" immune receptor functions.

Two unequally redundant "helper" immune receptor families mediate Arabidopsis thaliana intracellular "sensor" immune receptor functions.

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