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Robustness of plant quantitative disease resistance is provided by a decentralized immune network.

Identifieur interne : 000060 ( Main/Exploration ); précédent : 000059; suivant : 000061

Robustness of plant quantitative disease resistance is provided by a decentralized immune network.

Auteurs : Florent Delplace [France] ; Carine Huard-Chauveau [France] ; Ullrich Dubiella [France, Allemagne] ; Mehdi Khafif [France] ; Eva Alvarez [France] ; Gautier Langin [France] ; Fabrice Roux [France] ; Rémi Peyraud [France] ; Dominique Roby [France]

Source :

RBID : pubmed:32669441

Descripteurs français

English descriptors

Abstract

Quantitative disease resistance (QDR) represents the predominant form of resistance in natural populations and crops. Surprisingly, very limited information exists on the biomolecular network of the signaling machineries underlying this form of plant immunity. This lack of information may result from its complex and quantitative nature. Here, we used an integrative approach including genomics, network reconstruction, and mutational analysis to identify and validate molecular networks that control QDR in Arabidopsis thaliana in response to the bacterial pathogen Xanthomonas campestris To tackle this challenge, we first performed a transcriptomic analysis focused on the early stages of infection and using transgenic lines deregulated for the expression of RKS1, a gene underlying a QTL conferring quantitative and broad-spectrum resistance to XcampestrisRKS1-dependent gene expression was shown to involve multiple cellular activities (signaling, transport, and metabolism processes), mainly distinct from effector-triggered immunity (ETI) and pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) responses already characterized in Athaliana Protein-protein interaction network reconstitution then revealed a highly interconnected and distributed RKS1-dependent network, organized in five gene modules. Finally, knockout mutants for 41 genes belonging to the different functional modules of the network revealed that 76% of the genes and all gene modules participate partially in RKS1-mediated resistance. However, these functional modules exhibit differential robustness to genetic mutations, indicating that, within the decentralized structure of the QDR network, some modules are more resilient than others. In conclusion, our work sheds light on the complexity of QDR and provides comprehensive understanding of a QDR immune network.

DOI: 10.1073/pnas.2000078117
PubMed: 32669441
PubMed Central: PMC7395444


Affiliations:


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<keywords scheme="KwdEn" xml:lang="en">
<term>Computational Biology (methods)</term>
<term>Disease Resistance (immunology)</term>
<term>Disease Susceptibility (immunology)</term>
<term>Gene Expression Profiling (MeSH)</term>
<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Genes, Plant (MeSH)</term>
<term>Host-Pathogen Interactions (genetics)</term>
<term>Host-Pathogen Interactions (immunology)</term>
<term>Immunomodulation (MeSH)</term>
<term>Models, Biological (MeSH)</term>
<term>Phenotype (MeSH)</term>
<term>Plant Diseases (etiology)</term>
<term>Plant Immunity (MeSH)</term>
<term>Protein Interaction Mapping (MeSH)</term>
<term>Protein Interaction Maps (MeSH)</term>
<term>Transcriptome (MeSH)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Analyse de profil d'expression de gènes (MeSH)</term>
<term>Biologie informatique (méthodes)</term>
<term>Cartes d'interactions protéiques (MeSH)</term>
<term>Cartographie d'interactions entre protéines (MeSH)</term>
<term>Gènes de plante (MeSH)</term>
<term>Immunité des plantes (MeSH)</term>
<term>Immunomodulation (MeSH)</term>
<term>Interactions hôte-pathogène (génétique)</term>
<term>Interactions hôte-pathogène (immunologie)</term>
<term>Maladies des plantes (étiologie)</term>
<term>Modèles biologiques (MeSH)</term>
<term>Phénotype (MeSH)</term>
<term>Prédisposition aux maladies (immunologie)</term>
<term>Régulation de l'expression des gènes végétaux (MeSH)</term>
<term>Résistance à la maladie (immunologie)</term>
<term>Transcriptome (MeSH)</term>
</keywords>
<keywords scheme="MESH" qualifier="etiology" xml:lang="en">
<term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Host-Pathogen Interactions</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Interactions hôte-pathogène</term>
</keywords>
<keywords scheme="MESH" qualifier="immunologie" xml:lang="fr">
<term>Interactions hôte-pathogène</term>
<term>Prédisposition aux maladies</term>
<term>Résistance à la maladie</term>
</keywords>
<keywords scheme="MESH" qualifier="immunology" xml:lang="en">
<term>Disease Resistance</term>
<term>Disease Susceptibility</term>
<term>Host-Pathogen Interactions</term>
</keywords>
<keywords scheme="MESH" qualifier="methods" xml:lang="en">
<term>Computational Biology</term>
</keywords>
<keywords scheme="MESH" qualifier="méthodes" xml:lang="fr">
<term>Biologie informatique</term>
</keywords>
<keywords scheme="MESH" qualifier="étiologie" xml:lang="fr">
<term>Maladies des plantes</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Gene Expression Profiling</term>
<term>Gene Expression Regulation, Plant</term>
<term>Genes, Plant</term>
<term>Immunomodulation</term>
<term>Models, Biological</term>
<term>Phenotype</term>
<term>Plant Immunity</term>
<term>Protein Interaction Mapping</term>
<term>Protein Interaction Maps</term>
<term>Transcriptome</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Analyse de profil d'expression de gènes</term>
<term>Cartes d'interactions protéiques</term>
<term>Cartographie d'interactions entre protéines</term>
<term>Gènes de plante</term>
<term>Immunité des plantes</term>
<term>Immunomodulation</term>
<term>Modèles biologiques</term>
<term>Phénotype</term>
<term>Régulation de l'expression des gènes végétaux</term>
<term>Transcriptome</term>
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<front>
<div type="abstract" xml:lang="en">Quantitative disease resistance (QDR) represents the predominant form of resistance in natural populations and crops. Surprisingly, very limited information exists on the biomolecular network of the signaling machineries underlying this form of plant immunity. This lack of information may result from its complex and quantitative nature. Here, we used an integrative approach including genomics, network reconstruction, and mutational analysis to identify and validate molecular networks that control QDR in
<i>Arabidopsis thaliana</i>
in response to the bacterial pathogen
<i>Xanthomonas campestris</i>
To tackle this challenge, we first performed a transcriptomic analysis focused on the early stages of infection and using transgenic lines deregulated for the expression of
<i>RKS1</i>
, a gene underlying a QTL conferring quantitative and broad-spectrum resistance to
<i>X</i>
<i>campestris</i>
<i>RKS1</i>
-dependent gene expression was shown to involve multiple cellular activities (signaling, transport, and metabolism processes), mainly distinct from effector-triggered immunity (ETI) and pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) responses already characterized in
<i>A</i>
<i>thaliana</i>
Protein-protein interaction network reconstitution then revealed a highly interconnected and distributed RKS1-dependent network, organized in five gene modules. Finally, knockout mutants for 41 genes belonging to the different functional modules of the network revealed that 76% of the genes and all gene modules participate partially in RKS1-mediated resistance. However, these functional modules exhibit differential robustness to genetic mutations, indicating that, within the decentralized structure of the QDR network, some modules are more resilient than others. In conclusion, our work sheds light on the complexity of QDR and provides comprehensive understanding of a QDR immune network.</div>
</front>
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<Month>09</Month>
<Day>17</Day>
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<Month>09</Month>
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<Issue>30</Issue>
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<Title>Proceedings of the National Academy of Sciences of the United States of America</Title>
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<ArticleTitle>Robustness of plant quantitative disease resistance is provided by a decentralized immune network.</ArticleTitle>
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<Abstract>
<AbstractText>Quantitative disease resistance (QDR) represents the predominant form of resistance in natural populations and crops. Surprisingly, very limited information exists on the biomolecular network of the signaling machineries underlying this form of plant immunity. This lack of information may result from its complex and quantitative nature. Here, we used an integrative approach including genomics, network reconstruction, and mutational analysis to identify and validate molecular networks that control QDR in
<i>Arabidopsis thaliana</i>
in response to the bacterial pathogen
<i>Xanthomonas campestris</i>
To tackle this challenge, we first performed a transcriptomic analysis focused on the early stages of infection and using transgenic lines deregulated for the expression of
<i>RKS1</i>
, a gene underlying a QTL conferring quantitative and broad-spectrum resistance to
<i>X</i>
<i>campestris</i>
<i>RKS1</i>
-dependent gene expression was shown to involve multiple cellular activities (signaling, transport, and metabolism processes), mainly distinct from effector-triggered immunity (ETI) and pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) responses already characterized in
<i>A</i>
<i>thaliana</i>
Protein-protein interaction network reconstitution then revealed a highly interconnected and distributed RKS1-dependent network, organized in five gene modules. Finally, knockout mutants for 41 genes belonging to the different functional modules of the network revealed that 76% of the genes and all gene modules participate partially in RKS1-mediated resistance. However, these functional modules exhibit differential robustness to genetic mutations, indicating that, within the decentralized structure of the QDR network, some modules are more resilient than others. In conclusion, our work sheds light on the complexity of QDR and provides comprehensive understanding of a QDR immune network.</AbstractText>
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<LastName>Delplace</LastName>
<ForeName>Florent</ForeName>
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<Affiliation>Laboratoire des Interactions Plantes-Microorganismes, Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, CNRS, Université de Toulouse, 31326 Castanet-Tolosan, France.</Affiliation>
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<ForeName>Carine</ForeName>
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</AffiliationInfo>
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<ForeName>Ullrich</ForeName>
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<AffiliationInfo>
<Affiliation>Laboratoire des Interactions Plantes-Microorganismes, Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, CNRS, Université de Toulouse, 31326 Castanet-Tolosan, France.</Affiliation>
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<Affiliation>Laboratoire des Interactions Plantes-Microorganismes, Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, CNRS, Université de Toulouse, 31326 Castanet-Tolosan, France.</Affiliation>
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<LastName>Langin</LastName>
<ForeName>Gautier</ForeName>
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<AffiliationInfo>
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</AffiliationInfo>
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<LastName>Roux</LastName>
<ForeName>Fabrice</ForeName>
<Initials>F</Initials>
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</AffiliationInfo>
</Author>
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<LastName>Peyraud</LastName>
<ForeName>Rémi</ForeName>
<Initials>R</Initials>
<Identifier Source="ORCID">0000-0002-7580-042X</Identifier>
<AffiliationInfo>
<Affiliation>Laboratoire des Interactions Plantes-Microorganismes, Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, CNRS, Université de Toulouse, 31326 Castanet-Tolosan, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>iMean, 31520 Toulouse, France.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Roby</LastName>
<ForeName>Dominique</ForeName>
<Initials>D</Initials>
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<MeshHeading>
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<MeshHeading>
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<MeshHeading>
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<Keyword MajorTopicYN="Y">immunity</Keyword>
<Keyword MajorTopicYN="Y">plant pathogen interactions</Keyword>
<Keyword MajorTopicYN="Y">quantitative disease resistance</Keyword>
<Keyword MajorTopicYN="Y">regulatory networks</Keyword>
<Keyword MajorTopicYN="Y">systems biology</Keyword>
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<name sortKey="Delplace, Florent" sort="Delplace, Florent" uniqKey="Delplace F" first="Florent" last="Delplace">Florent Delplace</name>
</region>
<name sortKey="Alvarez, Eva" sort="Alvarez, Eva" uniqKey="Alvarez E" first="Eva" last="Alvarez">Eva Alvarez</name>
<name sortKey="Dubiella, Ullrich" sort="Dubiella, Ullrich" uniqKey="Dubiella U" first="Ullrich" last="Dubiella">Ullrich Dubiella</name>
<name sortKey="Huard Chauveau, Carine" sort="Huard Chauveau, Carine" uniqKey="Huard Chauveau C" first="Carine" last="Huard-Chauveau">Carine Huard-Chauveau</name>
<name sortKey="Khafif, Mehdi" sort="Khafif, Mehdi" uniqKey="Khafif M" first="Mehdi" last="Khafif">Mehdi Khafif</name>
<name sortKey="Langin, Gautier" sort="Langin, Gautier" uniqKey="Langin G" first="Gautier" last="Langin">Gautier Langin</name>
<name sortKey="Peyraud, Remi" sort="Peyraud, Remi" uniqKey="Peyraud R" first="Rémi" last="Peyraud">Rémi Peyraud</name>
<name sortKey="Peyraud, Remi" sort="Peyraud, Remi" uniqKey="Peyraud R" first="Rémi" last="Peyraud">Rémi Peyraud</name>
<name sortKey="Roby, Dominique" sort="Roby, Dominique" uniqKey="Roby D" first="Dominique" last="Roby">Dominique Roby</name>
<name sortKey="Roux, Fabrice" sort="Roux, Fabrice" uniqKey="Roux F" first="Fabrice" last="Roux">Fabrice Roux</name>
</country>
<country name="Allemagne">
<noRegion>
<name sortKey="Dubiella, Ullrich" sort="Dubiella, Ullrich" uniqKey="Dubiella U" first="Ullrich" last="Dubiella">Ullrich Dubiella</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>

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