PlantPathoEffV1, Main, Exploration, bibRecord, 000172

Evolution of a guarded decoy protease and its receptor in solanaceous plants.

Identifieur interne : 000172 ( Main/Exploration ); précédent : 000171; suivant : 000173

Evolution of a guarded decoy protease and its receptor in solanaceous plants.

Auteurs : Jiorgos Kourelis [Royaume-Uni] ; Shivani Malik [Royaume-Uni] ; Oliver Mattinson [Royaume-Uni] ; Sonja Krauter [Royaume-Uni] ; Parvinderdeep S. Kahlon [Royaume-Uni] ; Judith K. Paulus [Royaume-Uni] ; Renier A L. Van Der Hoorn [Royaume-Uni]

Source :

Nature communications [ 2041-1723 ] ; 2020.

RBID : pubmed:32879321

Descripteurs français

KwdFr :
- Cladosporium (génétique), Cladosporium (métabolisme), Cladosporium (pathogénicité), Gènes de plante (MeSH), Immunité des plantes (génétique), Inhibiteurs de protéases (métabolisme), Interactions hôte-parasite (MeSH), Maladies des plantes (microbiologie), Peptide hydrolases (génétique), Peptide hydrolases (métabolisme), Phylogenèse (MeSH), Protéines fongiques (métabolisme), Protéines végétales (génétique), Protéines végétales (métabolisme), Résistance à la maladie (génétique), Solanum (génétique), Solanum (microbiologie), Solanum (métabolisme), Tabac (génétique), Tabac (microbiologie), Tabac (métabolisme), Évolution moléculaire (MeSH).
MESH :
- génétique : Cladosporium, Immunité des plantes, Peptide hydrolases, Protéines végétales, Résistance à la maladie, Solanum, Tabac.
- microbiologie : Maladies des plantes, Solanum, Tabac.
- métabolisme : Cladosporium, Inhibiteurs de protéases, Peptide hydrolases, Protéines fongiques, Protéines végétales, Solanum, Tabac.
- pathogénicité : Cladosporium.
- Gènes de plante, Interactions hôte-parasite, Phylogenèse, Évolution moléculaire.

English descriptors

KwdEn :
- Cladosporium (genetics), Cladosporium (metabolism), Cladosporium (pathogenicity), Disease Resistance (genetics), Evolution, Molecular (MeSH), Fungal Proteins (metabolism), Genes, Plant (MeSH), Host-Parasite Interactions (MeSH), Peptide Hydrolases (genetics), Peptide Hydrolases (metabolism), Phylogeny (MeSH), Plant Diseases (microbiology), Plant Immunity (genetics), Plant Proteins (genetics), Plant Proteins (metabolism), Protease Inhibitors (metabolism), Solanum (genetics), Solanum (metabolism), Solanum (microbiology), Tobacco (genetics), Tobacco (metabolism), Tobacco (microbiology).
MESH :
- chemical , genetics : Peptide Hydrolases, Plant Proteins.
- chemical , metabolism : Fungal Proteins, Peptide Hydrolases, Plant Proteins, Protease Inhibitors.
- genetics : Cladosporium, Disease Resistance, Plant Immunity, Solanum, Tobacco.
- metabolism : Cladosporium, Solanum, Tobacco.
- microbiology : Plant Diseases, Solanum, Tobacco.
- pathogenicity : Cladosporium.
- Evolution, Molecular, Genes, Plant, Host-Parasite Interactions, Phylogeny.

Abstract

Rcr3 is a secreted protease of tomato that is targeted by fungal effector Avr2, a secreted protease inhibitor of the fungal pathogen Cladosporium fulvum. The Avr2-Rcr3 complex is recognized by receptor-like protein Cf-2, triggering hypersensitive cell death (HR) and disease resistance. Avr2 also targets Rcr3 paralog Pip1, which is not required for Avr2 recognition but contributes to basal resistance. Thus, Rcr3 acts as a guarded decoy in this interaction, trapping the fungus into a recognition event. Here we show that Rcr3 evolved > 50 million years ago (Mya), whereas Cf-2 evolved <6Mya by co-opting the pre-existing Rcr3 in the Solanum genus. Ancient Rcr3 homologs present in tomato, potato, eggplants, pepper, petunia and tobacco can be inhibited by Avr2 with the exception of tobacco Rcr3. Four variant residues in Rcr3 promote Avr2 inhibition, but the Rcr3 that co-evolved with Cf-2 lacks three of these residues, indicating that the Rcr3 co-receptor is suboptimal for Avr2 binding. Pepper Rcr3 triggers HR with Cf-2 and Avr2 when engineered for enhanced inhibition by Avr2. Nicotiana benthamiana (Nb) is a natural null mutant carrying Rcr3 and Pip1 alleles with deleterious frame-shift mutations. Resurrected NbRcr3 and NbPip1 alleles were active proteases and further NbRcr3 engineering facilitated Avr2 inhibition, uncoupled from HR signalling. The evolution of a receptor co-opting a conserved pathogen target contrasts with other indirect pathogen recognition mechanisms.

DOI: 10.1038/s41467-020-18069-5
PubMed: 32879321
PubMed Central: PMC7468133

Affiliations:

Links toward previous steps (curation, corpus...)

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Le document en format XML

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<term>Cladosporium (metabolism)</term>
<term>Cladosporium (pathogenicity)</term>
<term>Disease Resistance (genetics)</term>
<term>Evolution, Molecular (MeSH)</term>
<term>Fungal Proteins (metabolism)</term>
<term>Genes, Plant (MeSH)</term>
<term>Host-Parasite Interactions (MeSH)</term>
<term>Peptide Hydrolases (genetics)</term>
<term>Peptide Hydrolases (metabolism)</term>
<term>Phylogeny (MeSH)</term>
<term>Plant Diseases (microbiology)</term>
<term>Plant Immunity (genetics)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Protease Inhibitors (metabolism)</term>
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<term>Cladosporium (métabolisme)</term>
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<term>Gènes de plante (MeSH)</term>
<term>Immunité des plantes (génétique)</term>
<term>Inhibiteurs de protéases (métabolisme)</term>
<term>Interactions hôte-parasite (MeSH)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Peptide hydrolases (génétique)</term>
<term>Peptide hydrolases (métabolisme)</term>
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<term>Protéines végétales (métabolisme)</term>
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<term>Solanum (métabolisme)</term>
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<term>Tabac (microbiologie)</term>
<term>Tabac (métabolisme)</term>
<term>Évolution moléculaire (MeSH)</term>
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<term>Plant Proteins</term>
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<term>Peptide Hydrolases</term>
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<term>Protease Inhibitors</term>
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<term>Peptide hydrolases</term>
<term>Protéines végétales</term>
<term>Résistance à la maladie</term>
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<term>Tabac</term>
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<term>Protéines fongiques</term>
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<term>Host-Parasite Interactions</term>
<term>Phylogeny</term>
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<term>Interactions hôte-parasite</term>
<term>Phylogenèse</term>
<term>Évolution moléculaire</term>
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<front><div type="abstract" xml:lang="en">Rcr3 is a secreted protease of tomato that is targeted by fungal effector Avr2, a secreted protease inhibitor of the fungal pathogen Cladosporium fulvum. The Avr2-Rcr3 complex is recognized by receptor-like protein Cf-2, triggering hypersensitive cell death (HR) and disease resistance. Avr2 also targets Rcr3 paralog Pip1, which is not required for Avr2 recognition but contributes to basal resistance. Thus, Rcr3 acts as a guarded decoy in this interaction, trapping the fungus into a recognition event. Here we show that Rcr3 evolved > 50 million years ago (Mya), whereas Cf-2 evolved <6Mya by co-opting the pre-existing Rcr3 in the Solanum genus. Ancient Rcr3 homologs present in tomato, potato, eggplants, pepper, petunia and tobacco can be inhibited by Avr2 with the exception of tobacco Rcr3. Four variant residues in Rcr3 promote Avr2 inhibition, but the Rcr3 that co-evolved with Cf-2 lacks three of these residues, indicating that the Rcr3 co-receptor is suboptimal for Avr2 binding. Pepper Rcr3 triggers HR with Cf-2 and Avr2 when engineered for enhanced inhibition by Avr2. Nicotiana benthamiana (Nb) is a natural null mutant carrying Rcr3 and Pip1 alleles with deleterious frame-shift mutations. Resurrected NbRcr3 and NbPip1 alleles were active proteases and further NbRcr3 engineering facilitated Avr2 inhibition, uncoupled from HR signalling. The evolution of a receptor co-opting a conserved pathogen target contrasts with other indirect pathogen recognition mechanisms.</div>
</front>
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<Month>09</Month>
<Day>02</Day>
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<Title>Nature communications</Title>
<ISOAbbreviation>Nat Commun</ISOAbbreviation>
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<ELocationID EIdType="doi" ValidYN="Y">10.1038/s41467-020-18069-5</ELocationID>
<Abstract><AbstractText>Rcr3 is a secreted protease of tomato that is targeted by fungal effector Avr2, a secreted protease inhibitor of the fungal pathogen Cladosporium fulvum. The Avr2-Rcr3 complex is recognized by receptor-like protein Cf-2, triggering hypersensitive cell death (HR) and disease resistance. Avr2 also targets Rcr3 paralog Pip1, which is not required for Avr2 recognition but contributes to basal resistance. Thus, Rcr3 acts as a guarded decoy in this interaction, trapping the fungus into a recognition event. Here we show that Rcr3 evolved > 50 million years ago (Mya), whereas Cf-2 evolved <6Mya by co-opting the pre-existing Rcr3 in the Solanum genus. Ancient Rcr3 homologs present in tomato, potato, eggplants, pepper, petunia and tobacco can be inhibited by Avr2 with the exception of tobacco Rcr3. Four variant residues in Rcr3 promote Avr2 inhibition, but the Rcr3 that co-evolved with Cf-2 lacks three of these residues, indicating that the Rcr3 co-receptor is suboptimal for Avr2 binding. Pepper Rcr3 triggers HR with Cf-2 and Avr2 when engineered for enhanced inhibition by Avr2. Nicotiana benthamiana (Nb) is a natural null mutant carrying Rcr3 and Pip1 alleles with deleterious frame-shift mutations. Resurrected NbRcr3 and NbPip1 alleles were active proteases and further NbRcr3 engineering facilitated Avr2 inhibition, uncoupled from HR signalling. The evolution of a receptor co-opting a conserved pathogen target contrasts with other indirect pathogen recognition mechanisms.</AbstractText>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Kourelis</LastName>
<ForeName>Jiorgos</ForeName>
<Initials>J</Initials>
<Identifier Source="ORCID">0000-0002-9007-1333</Identifier>
<AffiliationInfo><Affiliation>Plant Chemetics Laboratory, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB, Oxford, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Malik</LastName>
<ForeName>Shivani</ForeName>
<Initials>S</Initials>
<AffiliationInfo><Affiliation>Plant Chemetics Laboratory, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB, Oxford, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Mattinson</LastName>
<ForeName>Oliver</ForeName>
<Initials>O</Initials>
<Identifier Source="ORCID">0000-0001-8374-0837</Identifier>
<AffiliationInfo><Affiliation>Plant Chemetics Laboratory, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB, Oxford, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Krauter</LastName>
<ForeName>Sonja</ForeName>
<Initials>S</Initials>
<AffiliationInfo><Affiliation>Plant Chemetics Laboratory, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB, Oxford, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Kahlon</LastName>
<ForeName>Parvinderdeep S</ForeName>
<Initials>PS</Initials>
<AffiliationInfo><Affiliation>Plant Chemetics Laboratory, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB, Oxford, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Paulus</LastName>
<ForeName>Judith K</ForeName>
<Initials>JK</Initials>
<AffiliationInfo><Affiliation>Plant Chemetics Laboratory, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB, Oxford, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>van der Hoorn</LastName>
<ForeName>Renier A L</ForeName>
<Initials>RAL</Initials>
<Identifier Source="ORCID">0000-0002-3692-7487</Identifier>
<AffiliationInfo><Affiliation>Plant Chemetics Laboratory, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB, Oxford, UK. renier.vanderhoorn@plants.ox.ac.uk.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<GrantList CompleteYN="Y"><Grant><GrantID>BB/S003193/1</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>02</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo><Country>England</Country>
<MedlineTA>Nat Commun</MedlineTA>
<NlmUniqueID>101528555</NlmUniqueID>
<ISSNLinking>2041-1723</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList><Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D005656">Fungal Proteins</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D011480">Protease Inhibitors</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>EC 3.4.-</RegistryNumber>
<NameOfSubstance UI="D010447">Peptide Hydrolases</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList><MeshHeading><DescriptorName UI="D002963" MajorTopicYN="Y">Cladosporium</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000472" MajorTopicYN="N">pathogenicity</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D060467" MajorTopicYN="N">Disease Resistance</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D019143" MajorTopicYN="N">Evolution, Molecular</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D005656" MajorTopicYN="N">Fungal Proteins</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D017343" MajorTopicYN="N">Genes, Plant</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D006790" MajorTopicYN="N">Host-Parasite Interactions</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010447" MajorTopicYN="N">Peptide Hydrolases</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010802" MajorTopicYN="N">Phylogeny</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D057865" MajorTopicYN="N">Plant Immunity</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D011480" MajorTopicYN="N">Protease Inhibitors</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D032322" MajorTopicYN="Y">Solanum</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D014026" MajorTopicYN="Y">Tobacco</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
</MeshHeadingList>
</MedlineCitation>
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<Month>03</Month>
<Day>26</Day>
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<PubMedPubDate PubStatus="accepted"><Year>2020</Year>
<Month>08</Month>
<Day>03</Day>
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<Day>4</Day>
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	Serveur d'exploration sur les effecteurs de phytopathogènes
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Serveur d'exploration sur les effecteurs de phytopathogènes

Evolution of a guarded decoy protease and its receptor in solanaceous plants.

Evolution of a guarded decoy protease and its receptor in solanaceous plants.

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