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Functional Divergence of Two Secreted Immune Proteases of Tomato.

Identifieur interne : 000E62 ( Main/Exploration ); précédent : 000E61; suivant : 000E63

Functional Divergence of Two Secreted Immune Proteases of Tomato.

Auteurs : Muhammad Ilyas [Allemagne] ; Anja C. Hörger [Allemagne] ; Tolga O. Bozkurt [Royaume-Uni] ; Harrold A. Van Den Burg [Pays-Bas] ; Farnusch Kaschani [Allemagne] ; Markus Kaiser [Allemagne] ; Khaoula Belhaj [Royaume-Uni] ; Matthew Smoker [Royaume-Uni] ; Matthieu H A J. Joosten [Pays-Bas] ; Sophien Kamoun [Royaume-Uni] ; Renier A L. Van Der Hoorn [Allemagne]

Source :

RBID : pubmed:26299516

Descripteurs français

English descriptors

Abstract

Rcr3 and Pip1 are paralogous secreted papain-like proteases of tomato. Both proteases are inhibited by Avr2 from the fungal pathogen Cladosporium fulvum, but only Rcr3 acts as a co-receptor for Avr2 recognition by the tomato Cf-2 immune receptor. Here, we show that Pip1-depleted tomato plants are hyper-susceptible to fungal, bacterial, and oomycete plant pathogens, demonstrating that Pip1 is an important broad-range immune protease. By contrast, in the absence of Cf-2, Rcr3 depletion does not affect fungal and bacterial infection levels but causes increased susceptibility only to the oomycete pathogen Phytophthora infestans. Rcr3 and Pip1 reside on a genetic locus that evolved over 36 million years ago. These proteins differ in surface-exposed residues outside the substrate-binding groove, and Pip1 is 5- to 10-fold more abundant than Rcr3. We propose a model in which Rcr3 and Pip1 diverged functionally upon gene duplication, possibly driven by an arms race with pathogen-derived inhibitors or by coevolution with the Cf-2 immune receptor detecting inhibitors of Rcr3, but not of Pip1.

DOI: 10.1016/j.cub.2015.07.030
PubMed: 26299516


Affiliations:


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Le document en format XML

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<term>Cladosporium (physiology)</term>
<term>Evolution, Molecular (MeSH)</term>
<term>Gene Duplication (MeSH)</term>
<term>Lycopersicon esculentum (genetics)</term>
<term>Lycopersicon esculentum (immunology)</term>
<term>Lycopersicon esculentum (metabolism)</term>
<term>Peptide Hydrolases (genetics)</term>
<term>Peptide Hydrolases (metabolism)</term>
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<term>Plant Proteins (metabolism)</term>
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<term>Cladosporium (physiologie)</term>
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<term>Lycopersicon esculentum (immunologie)</term>
<term>Lycopersicon esculentum (métabolisme)</term>
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<term>Peptide hydrolases (métabolisme)</term>
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<term>Protéines végétales (génétique)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Évolution moléculaire (MeSH)</term>
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<term>Peptide Hydrolases</term>
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Lycopersicon esculentum</term>
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<term>Protéines végétales</term>
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<term>Cladosporium</term>
<term>Phytophthora infestans</term>
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<term>Phytophthora infestans</term>
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<term>Evolution, Molecular</term>
<term>Gene Duplication</term>
</keywords>
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<term>Duplication de gène</term>
<term>Évolution moléculaire</term>
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<div type="abstract" xml:lang="en">Rcr3 and Pip1 are paralogous secreted papain-like proteases of tomato. Both proteases are inhibited by Avr2 from the fungal pathogen Cladosporium fulvum, but only Rcr3 acts as a co-receptor for Avr2 recognition by the tomato Cf-2 immune receptor. Here, we show that Pip1-depleted tomato plants are hyper-susceptible to fungal, bacterial, and oomycete plant pathogens, demonstrating that Pip1 is an important broad-range immune protease. By contrast, in the absence of Cf-2, Rcr3 depletion does not affect fungal and bacterial infection levels but causes increased susceptibility only to the oomycete pathogen Phytophthora infestans. Rcr3 and Pip1 reside on a genetic locus that evolved over 36 million years ago. These proteins differ in surface-exposed residues outside the substrate-binding groove, and Pip1 is 5- to 10-fold more abundant than Rcr3. We propose a model in which Rcr3 and Pip1 diverged functionally upon gene duplication, possibly driven by an arms race with pathogen-derived inhibitors or by coevolution with the Cf-2 immune receptor detecting inhibitors of Rcr3, but not of Pip1.</div>
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<Journal>
<ISSN IssnType="Electronic">1879-0445</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>25</Volume>
<Issue>17</Issue>
<PubDate>
<Year>2015</Year>
<Month>Aug</Month>
<Day>31</Day>
</PubDate>
</JournalIssue>
<Title>Current biology : CB</Title>
<ISOAbbreviation>Curr Biol</ISOAbbreviation>
</Journal>
<ArticleTitle>Functional Divergence of Two Secreted Immune Proteases of Tomato.</ArticleTitle>
<Pagination>
<MedlinePgn>2300-6</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1016/j.cub.2015.07.030</ELocationID>
<ELocationID EIdType="pii" ValidYN="Y">S0960-9822(15)00833-7</ELocationID>
<Abstract>
<AbstractText>Rcr3 and Pip1 are paralogous secreted papain-like proteases of tomato. Both proteases are inhibited by Avr2 from the fungal pathogen Cladosporium fulvum, but only Rcr3 acts as a co-receptor for Avr2 recognition by the tomato Cf-2 immune receptor. Here, we show that Pip1-depleted tomato plants are hyper-susceptible to fungal, bacterial, and oomycete plant pathogens, demonstrating that Pip1 is an important broad-range immune protease. By contrast, in the absence of Cf-2, Rcr3 depletion does not affect fungal and bacterial infection levels but causes increased susceptibility only to the oomycete pathogen Phytophthora infestans. Rcr3 and Pip1 reside on a genetic locus that evolved over 36 million years ago. These proteins differ in surface-exposed residues outside the substrate-binding groove, and Pip1 is 5- to 10-fold more abundant than Rcr3. We propose a model in which Rcr3 and Pip1 diverged functionally upon gene duplication, possibly driven by an arms race with pathogen-derived inhibitors or by coevolution with the Cf-2 immune receptor detecting inhibitors of Rcr3, but not of Pip1.</AbstractText>
<CopyrightInformation>Copyright © 2015 Elsevier Ltd. All rights reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Ilyas</LastName>
<ForeName>Muhammad</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Plant Chemetics Laboratory, Max Planck Institute for Plant Breeding Research, Carl-von-Linné Weg 10, 50829 Cologne, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Hörger</LastName>
<ForeName>Anja C</ForeName>
<Initials>AC</Initials>
<AffiliationInfo>
<Affiliation>Plant Chemetics Laboratory, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB Oxford, UK; Plant Chemetics Laboratory, Max Planck Institute for Plant Breeding Research, Carl-von-Linné Weg 10, 50829 Cologne, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Bozkurt</LastName>
<ForeName>Tolga O</ForeName>
<Initials>TO</Initials>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, NR4 7UH Norwich, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>van den Burg</LastName>
<ForeName>Harrold A</ForeName>
<Initials>HA</Initials>
<AffiliationInfo>
<Affiliation>Molecular Plant Pathology, Swammerdam Institute for Life Sciences, University of Amsterdam, Science Park 904, 1098 XH Amsterdam, the Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kaschani</LastName>
<ForeName>Farnusch</ForeName>
<Initials>F</Initials>
<AffiliationInfo>
<Affiliation>Chemical Biology, Fakultät für Biologie, Zentrum für Medizinische Biotechnologie, Universität Duisburg-Essen, Universitätstr. 2, 45117 Essen, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kaiser</LastName>
<ForeName>Markus</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Chemical Biology, Fakultät für Biologie, Zentrum für Medizinische Biotechnologie, Universität Duisburg-Essen, Universitätstr. 2, 45117 Essen, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Belhaj</LastName>
<ForeName>Khaoula</ForeName>
<Initials>K</Initials>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, NR4 7UH Norwich, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Smoker</LastName>
<ForeName>Matthew</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, NR4 7UH Norwich, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Joosten</LastName>
<ForeName>Matthieu H A J</ForeName>
<Initials>MH</Initials>
<AffiliationInfo>
<Affiliation>SOL Group, Laboratory of Phytopathology, Droevendaalsesteeg 1, 6708 PB Wageningen, the Netherlands.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kamoun</LastName>
<ForeName>Sophien</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, Norwich Research Park, NR4 7UH Norwich, UK.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>van der Hoorn</LastName>
<ForeName>Renier A L</ForeName>
<Initials>RA</Initials>
<AffiliationInfo>
<Affiliation>Plant Chemetics Laboratory, Department of Plant Sciences, University of Oxford, South Parks Road, OX1 3RB Oxford, UK; Plant Chemetics Laboratory, Max Planck Institute for Plant Breeding Research, Carl-von-Linné Weg 10, 50829 Cologne, Germany. Electronic address: renier.vanderhoorn@plants.ox.ac.uk.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2015</Year>
<Month>08</Month>
<Day>20</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>England</Country>
<MedlineTA>Curr Biol</MedlineTA>
<NlmUniqueID>9107782</NlmUniqueID>
<ISSNLinking>0960-9822</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010940">Plant Proteins</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="N">Cladosporium</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D019143" MajorTopicYN="Y">Evolution, Molecular</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D020440" MajorTopicYN="N">Gene Duplication</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018551" MajorTopicYN="N">Lycopersicon esculentum</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</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="D055750" MajorTopicYN="N">Phytophthora infestans</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">Cladosporium fulvum</Keyword>
<Keyword MajorTopicYN="N">Cys protease</Keyword>
<Keyword MajorTopicYN="N">Phytophthora infestans</Keyword>
<Keyword MajorTopicYN="N">apoplast</Keyword>
<Keyword MajorTopicYN="N">immunity</Keyword>
<Keyword MajorTopicYN="N">tomato</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="received">
<Year>2015</Year>
<Month>05</Month>
<Day>29</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="revised">
<Year>2015</Year>
<Month>06</Month>
<Day>19</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2015</Year>
<Month>07</Month>
<Day>10</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2015</Year>
<Month>8</Month>
<Day>25</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed">
<Year>2015</Year>
<Month>8</Month>
<Day>25</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2016</Year>
<Month>6</Month>
<Day>9</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">26299516</ArticleId>
<ArticleId IdType="pii">S0960-9822(15)00833-7</ArticleId>
<ArticleId IdType="doi">10.1016/j.cub.2015.07.030</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
<affiliations>
<list>
<country>
<li>Allemagne</li>
<li>Pays-Bas</li>
<li>Royaume-Uni</li>
</country>
<region>
<li>District de Cologne</li>
<li>Hollande-Septentrionale</li>
<li>Rhénanie-du-Nord-Westphalie</li>
</region>
<settlement>
<li>Amsterdam</li>
<li>Cologne</li>
</settlement>
<orgName>
<li>Université d'Amsterdam</li>
<li>Université d'Oxford</li>
</orgName>
</list>
<tree>
<country name="Allemagne">
<region name="Rhénanie-du-Nord-Westphalie">
<name sortKey="Ilyas, Muhammad" sort="Ilyas, Muhammad" uniqKey="Ilyas M" first="Muhammad" last="Ilyas">Muhammad Ilyas</name>
</region>
<name sortKey="Horger, Anja C" sort="Horger, Anja C" uniqKey="Horger A" first="Anja C" last="Hörger">Anja C. Hörger</name>
<name sortKey="Kaiser, Markus" sort="Kaiser, Markus" uniqKey="Kaiser M" first="Markus" last="Kaiser">Markus Kaiser</name>
<name sortKey="Kaschani, Farnusch" sort="Kaschani, Farnusch" uniqKey="Kaschani F" first="Farnusch" last="Kaschani">Farnusch Kaschani</name>
<name sortKey="Van Der Hoorn, Renier A L" sort="Van Der Hoorn, Renier A L" uniqKey="Van Der Hoorn R" first="Renier A L" last="Van Der Hoorn">Renier A L. Van Der Hoorn</name>
</country>
<country name="Royaume-Uni">
<noRegion>
<name sortKey="Bozkurt, Tolga O" sort="Bozkurt, Tolga O" uniqKey="Bozkurt T" first="Tolga O" last="Bozkurt">Tolga O. Bozkurt</name>
</noRegion>
<name sortKey="Belhaj, Khaoula" sort="Belhaj, Khaoula" uniqKey="Belhaj K" first="Khaoula" last="Belhaj">Khaoula Belhaj</name>
<name sortKey="Kamoun, Sophien" sort="Kamoun, Sophien" uniqKey="Kamoun S" first="Sophien" last="Kamoun">Sophien Kamoun</name>
<name sortKey="Smoker, Matthew" sort="Smoker, Matthew" uniqKey="Smoker M" first="Matthew" last="Smoker">Matthew Smoker</name>
</country>
<country name="Pays-Bas">
<region name="Hollande-Septentrionale">
<name sortKey="Van Den Burg, Harrold A" sort="Van Den Burg, Harrold A" uniqKey="Van Den Burg H" first="Harrold A" last="Van Den Burg">Harrold A. Van Den Burg</name>
</region>
<name sortKey="Joosten, Matthieu H A J" sort="Joosten, Matthieu H A J" uniqKey="Joosten M" first="Matthieu H A J" last="Joosten">Matthieu H A J. Joosten</name>
</country>
</tree>
</affiliations>
</record>

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