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Extracellular proteolytic cascade in tomato activates immune protease Rcr3.

Identifieur interne : 000169 ( Main/Exploration ); précédent : 000168; suivant : 000170

Extracellular proteolytic cascade in tomato activates immune protease Rcr3.

Auteurs : Judith K. Paulus [Royaume-Uni] ; Jiorgos Kourelis [Royaume-Uni] ; Selva Ramasubramanian [Allemagne] ; Felix Homma [Royaume-Uni] ; Alice Godson [Royaume-Uni] ; Anja C. Hörger [Allemagne] ; Tram Ngoc Hong [Royaume-Uni, Allemagne] ; Daniel Krahn [Royaume-Uni] ; Laura Ossorio Carballo [Royaume-Uni] ; Shuaishuai Wang [République populaire de Chine] ; Joe Win [Royaume-Uni] ; Matthew Smoker [Royaume-Uni] ; Sophien Kamoun [Royaume-Uni] ; Suomeng Dong [République populaire de Chine] ; Renier A L. Van Der Hoorn [Royaume-Uni, Allemagne]

Source :

RBID : pubmed:32616567

Descripteurs français

English descriptors

Abstract

Proteolytic cascades regulate immunity and development in animals, but these cascades in plants have not yet been reported. Here we report that the extracellular immune protease Rcr3 of tomato is activated by P69B and other subtilases (SBTs), revealing a proteolytic cascade regulating extracellular immunity in solanaceous plants. Rcr3 is a secreted papain-like Cys protease (PLCP) of tomato that acts both in basal resistance against late blight disease (Phytophthora infestans) and in gene-for-gene resistance against the fungal pathogen Cladosporium fulvum (syn. Passalora fulva) Despite the prevalent model that Rcr3-like proteases can activate themselves at low pH, we found that catalytically inactive proRcr3 mutant precursors are still processed into mature mRcr3 isoforms. ProRcr3 is processed by secreted P69B and other Asp-selective SBTs in solanaceous plants, providing robust immunity through SBT redundancy. The apoplastic effector EPI1 of P. infestans can block Rcr3 activation by inhibiting SBTs, suggesting that this effector promotes virulence indirectly by preventing the activation of Rcr3(-like) immune proteases. Rcr3 activation in Nicotiana benthamiana requires a SBT from a different subfamily, indicating that extracellular proteolytic cascades have evolved convergently in solanaceous plants or are very ancient in the plant kingdom. The frequent incidence of Asp residues in the cleavage region of Rcr3-like proteases in solanaceous plants indicates that activation of immune proteases by SBTs is a general mechanism, illuminating a proteolytic cascade that provides robust apoplastic immunity.

DOI: 10.1073/pnas.1921101117
PubMed: 32616567
PubMed Central: PMC7382257


Affiliations:


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Le document en format XML

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<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>
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<title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
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<term>Cladosporium (MeSH)</term>
<term>Lycopersicon esculentum (genetics)</term>
<term>Lycopersicon esculentum (metabolism)</term>
<term>Peptide Hydrolases (genetics)</term>
<term>Peptide Hydrolases (metabolism)</term>
<term>Phytophthora infestans (MeSH)</term>
<term>Plant Diseases (immunology)</term>
<term>Plant Diseases (parasitology)</term>
<term>Plant Diseases (prevention & control)</term>
<term>Plant Immunity (MeSH)</term>
<term>Plant Proteins (metabolism)</term>
<term>Protein Isoforms (MeSH)</term>
<term>Proteolysis (MeSH)</term>
<term>Virulence (MeSH)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Cladosporium (MeSH)</term>
<term>Immunité des plantes (MeSH)</term>
<term>Isoformes de protéines (MeSH)</term>
<term>Lycopersicon esculentum (génétique)</term>
<term>Lycopersicon esculentum (métabolisme)</term>
<term>Maladies des plantes (immunologie)</term>
<term>Maladies des plantes (parasitologie)</term>
<term>Maladies des plantes (prévention et contrôle)</term>
<term>Peptide hydrolases (génétique)</term>
<term>Peptide hydrolases (métabolisme)</term>
<term>Phytophthora infestans (MeSH)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Protéolyse (MeSH)</term>
<term>Virulence (MeSH)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>Peptide Hydrolases</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Lycopersicon esculentum</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Lycopersicon esculentum</term>
<term>Peptide hydrolases</term>
</keywords>
<keywords scheme="MESH" qualifier="immunologie" xml:lang="fr">
<term>Maladies des plantes</term>
</keywords>
<keywords scheme="MESH" qualifier="immunology" xml:lang="en">
<term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Lycopersicon esculentum</term>
<term>Peptide Hydrolases</term>
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Lycopersicon esculentum</term>
<term>Peptide hydrolases</term>
<term>Protéines végétales</term>
</keywords>
<keywords scheme="MESH" qualifier="parasitologie" xml:lang="fr">
<term>Maladies des plantes</term>
</keywords>
<keywords scheme="MESH" qualifier="parasitology" xml:lang="en">
<term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" qualifier="prevention & control" xml:lang="en">
<term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" qualifier="prévention et contrôle" xml:lang="fr">
<term>Maladies des plantes</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Cladosporium</term>
<term>Phytophthora infestans</term>
<term>Plant Immunity</term>
<term>Protein Isoforms</term>
<term>Proteolysis</term>
<term>Virulence</term>
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<term>Cladosporium</term>
<term>Immunité des plantes</term>
<term>Isoformes de protéines</term>
<term>Phytophthora infestans</term>
<term>Protéolyse</term>
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<div type="abstract" xml:lang="en">Proteolytic cascades regulate immunity and development in animals, but these cascades in plants have not yet been reported. Here we report that the extracellular immune protease Rcr3 of tomato is activated by P69B and other subtilases (SBTs), revealing a proteolytic cascade regulating extracellular immunity in solanaceous plants. Rcr3 is a secreted papain-like Cys protease (PLCP) of tomato that acts both in basal resistance against late blight disease (
<i>Phytophthora infestans</i>
) and in gene-for-gene resistance against the fungal pathogen
<i>Cladosporium fulvum (</i>
syn.
<i>Passalora fulva)</i>
Despite the prevalent model that Rcr3-like proteases can activate themselves at low pH, we found that catalytically inactive proRcr3 mutant precursors are still processed into mature mRcr3 isoforms. ProRcr3 is processed by secreted P69B and other Asp-selective SBTs in solanaceous plants, providing robust immunity through SBT redundancy. The apoplastic effector EPI1 of
<i>P. infestans</i>
can block Rcr3 activation by inhibiting SBTs, suggesting that this effector promotes virulence indirectly by preventing the activation of Rcr3(-like) immune proteases. Rcr3 activation in
<i>Nicotiana benthamiana</i>
requires a SBT from a different subfamily, indicating that extracellular proteolytic cascades have evolved convergently in solanaceous plants or are very ancient in the plant kingdom. The frequent incidence of Asp residues in the cleavage region of Rcr3-like proteases in solanaceous plants indicates that activation of immune proteases by SBTs is a general mechanism, illuminating a proteolytic cascade that provides robust apoplastic immunity.</div>
</front>
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<DateCompleted>
<Year>2020</Year>
<Month>09</Month>
<Day>14</Day>
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<Year>2020</Year>
<Month>09</Month>
<Day>14</Day>
</DateRevised>
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<ISSN IssnType="Electronic">1091-6490</ISSN>
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<Volume>117</Volume>
<Issue>29</Issue>
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<Year>2020</Year>
<Month>07</Month>
<Day>21</Day>
</PubDate>
</JournalIssue>
<Title>Proceedings of the National Academy of Sciences of the United States of America</Title>
<ISOAbbreviation>Proc Natl Acad Sci U S A</ISOAbbreviation>
</Journal>
<ArticleTitle>Extracellular proteolytic cascade in tomato activates immune protease Rcr3.</ArticleTitle>
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<MedlinePgn>17409-17417</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1073/pnas.1921101117</ELocationID>
<Abstract>
<AbstractText>Proteolytic cascades regulate immunity and development in animals, but these cascades in plants have not yet been reported. Here we report that the extracellular immune protease Rcr3 of tomato is activated by P69B and other subtilases (SBTs), revealing a proteolytic cascade regulating extracellular immunity in solanaceous plants. Rcr3 is a secreted papain-like Cys protease (PLCP) of tomato that acts both in basal resistance against late blight disease (
<i>Phytophthora infestans</i>
) and in gene-for-gene resistance against the fungal pathogen
<i>Cladosporium fulvum (</i>
syn.
<i>Passalora fulva)</i>
Despite the prevalent model that Rcr3-like proteases can activate themselves at low pH, we found that catalytically inactive proRcr3 mutant precursors are still processed into mature mRcr3 isoforms. ProRcr3 is processed by secreted P69B and other Asp-selective SBTs in solanaceous plants, providing robust immunity through SBT redundancy. The apoplastic effector EPI1 of
<i>P. infestans</i>
can block Rcr3 activation by inhibiting SBTs, suggesting that this effector promotes virulence indirectly by preventing the activation of Rcr3(-like) immune proteases. Rcr3 activation in
<i>Nicotiana benthamiana</i>
requires a SBT from a different subfamily, indicating that extracellular proteolytic cascades have evolved convergently in solanaceous plants or are very ancient in the plant kingdom. The frequent incidence of Asp residues in the cleavage region of Rcr3-like proteases in solanaceous plants indicates that activation of immune proteases by SBTs is a general mechanism, illuminating a proteolytic cascade that provides robust apoplastic immunity.</AbstractText>
<CopyrightInformation>Copyright © 2020 the Author(s). Published by PNAS.</CopyrightInformation>
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<LastName>Paulus</LastName>
<ForeName>Judith K</ForeName>
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<ForeName>Suomeng</ForeName>
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<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China.</Affiliation>
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<Keyword MajorTopicYN="Y">apoplast</Keyword>
<Keyword MajorTopicYN="Y">immunity</Keyword>
<Keyword MajorTopicYN="Y">proteolytic cascade</Keyword>
<Keyword MajorTopicYN="Y">subtilase</Keyword>
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