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Pathogen manipulation of chloroplast function triggers a light-dependent immune recognition.

Identifieur interne : 000098 ( Main/Exploration ); précédent : 000097; suivant : 000099

Pathogen manipulation of chloroplast function triggers a light-dependent immune recognition.

Auteurs : Chuyun Gao [République populaire de Chine] ; Huawei Xu [République populaire de Chine] ; Jie Huang [République populaire de Chine] ; Biying Sun [République populaire de Chine] ; Fan Zhang [République populaire de Chine] ; Zachary Savage [Royaume-Uni] ; Cian Duggan [Royaume-Uni] ; Tingxiu Yan [République populaire de Chine] ; Chih-Hang Wu [Royaume-Uni] ; Yuanchao Wang [République populaire de Chine] ; Vivianne G A A. Vleeshouwers [Pays-Bas] ; Sophien Kamoun [Royaume-Uni] ; Tolga O. Bozkurt [Royaume-Uni] ; Suomeng Dong [République populaire de Chine, Royaume-Uni]

Source :

RBID : pubmed:32284406

Descripteurs français

English descriptors

Abstract

In plants and animals, nucleotide-binding leucine-rich repeat (NLR) proteins are intracellular immune sensors that recognize and eliminate a wide range of invading pathogens. NLR-mediated immunity is known to be modulated by environmental factors. However, how pathogen recognition by NLRs is influenced by environmental factors such as light remains unclear. Here, we show that the agronomically important NLR Rpi-vnt1.1 requires light to confer disease resistance against races of the Irish potato famine pathogen Phytophthora infestans that secrete the effector protein AVRvnt1. The activation of Rpi-vnt1.1 requires a nuclear-encoded chloroplast protein, glycerate 3-kinase (GLYK), implicated in energy production. The pathogen effector AVRvnt1 binds the full-length chloroplast-targeted GLYK isoform leading to activation of Rpi-vnt1.1. In the dark, Rpi-vnt1.1-mediated resistance is compromised because plants produce a shorter GLYK-lacking the intact chloroplast transit peptide-that is not bound by AVRvnt1. The transition between full-length and shorter plant GLYK transcripts is controlled by a light-dependent alternative promoter selection mechanism. In plants that lack Rpi-vnt1.1, the presence of AVRvnt1 reduces GLYK accumulation in chloroplasts counteracting GLYK contribution to basal immunity. Our findings revealed that pathogen manipulation of chloroplast functions has resulted in a light-dependent immune response.

DOI: 10.1073/pnas.2002759117
PubMed: 32284406
PubMed Central: PMC7196767


Affiliations:


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Le document en format XML

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<name sortKey="Sun, Biying" sort="Sun, Biying" uniqKey="Sun B" first="Biying" last="Sun">Biying Sun</name>
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<name sortKey="Zhang, Fan" sort="Zhang, Fan" uniqKey="Zhang F" first="Fan" last="Zhang">Fan Zhang</name>
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<name sortKey="Savage, Zachary" sort="Savage, Zachary" uniqKey="Savage Z" first="Zachary" last="Savage">Zachary Savage</name>
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<nlm:affiliation>Imperial College, South Kensington Campus, SW7 2AZ London, United Kingdom.</nlm:affiliation>
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<name sortKey="Duggan, Cian" sort="Duggan, Cian" uniqKey="Duggan C" first="Cian" last="Duggan">Cian Duggan</name>
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<nlm:affiliation>Imperial College, South Kensington Campus, SW7 2AZ London, United Kingdom.</nlm:affiliation>
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<name sortKey="Yan, Tingxiu" sort="Yan, Tingxiu" uniqKey="Yan T" first="Tingxiu" last="Yan">Tingxiu Yan</name>
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<nlm:affiliation>College of Plant Protection, Nanjing Agricultural University, 210095 Nanjing, China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
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<name sortKey="Wu, Chih Hang" sort="Wu, Chih Hang" uniqKey="Wu C" first="Chih-Hang" last="Wu">Chih-Hang Wu</name>
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<name sortKey="Wang, Yuanchao" sort="Wang, Yuanchao" uniqKey="Wang Y" first="Yuanchao" last="Wang">Yuanchao Wang</name>
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<nlm:affiliation>Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China.</nlm:affiliation>
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<name sortKey="Vleeshouwers, Vivianne G A A" sort="Vleeshouwers, Vivianne G A A" uniqKey="Vleeshouwers V" first="Vivianne G A A" last="Vleeshouwers">Vivianne G A A. Vleeshouwers</name>
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<nlm:affiliation>Wageningen University and Research Plant Breeding, Wageningen University and Research, Wageningen 6708 PB, The Netherlands.</nlm:affiliation>
<country xml:lang="fr">Pays-Bas</country>
<wicri:regionArea>Wageningen University and Research Plant Breeding, Wageningen University and Research, Wageningen 6708 PB</wicri:regionArea>
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<name sortKey="Kamoun, Sophien" sort="Kamoun, Sophien" uniqKey="Kamoun S" first="Sophien" last="Kamoun">Sophien Kamoun</name>
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<nlm:affiliation>The Sainsbury Laboratory, University of East Anglia, NR4 7UH Norwich, United Kingdom.</nlm:affiliation>
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<name sortKey="Bozkurt, Tolga O" sort="Bozkurt, Tolga O" uniqKey="Bozkurt T" first="Tolga O" last="Bozkurt">Tolga O. Bozkurt</name>
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<nlm:affiliation>Imperial College, South Kensington Campus, SW7 2AZ London, United Kingdom.</nlm:affiliation>
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<name sortKey="Dong, Suomeng" sort="Dong, Suomeng" uniqKey="Dong S" first="Suomeng" last="Dong">Suomeng Dong</name>
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<nlm:affiliation>Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China.</nlm:affiliation>
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<series>
<title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
<idno type="eISSN">1091-6490</idno>
<imprint>
<date when="2020" type="published">2020</date>
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<textClass>
<keywords scheme="KwdEn" xml:lang="en">
<term>Agrobacterium (metabolism)</term>
<term>Animals (MeSH)</term>
<term>Chloroplasts (metabolism)</term>
<term>Chloroplasts (microbiology)</term>
<term>Escherichia coli (metabolism)</term>
<term>Fungal Proteins (MeSH)</term>
<term>Gene Expression Regulation, Enzymologic (MeSH)</term>
<term>Gene Expression Regulation, Plant (immunology)</term>
<term>Gene Expression Regulation, Plant (radiation effects)</term>
<term>Gene Silencing (MeSH)</term>
<term>Light (MeSH)</term>
<term>Microscopy, Confocal (MeSH)</term>
<term>NLR Proteins (genetics)</term>
<term>NLR Proteins (metabolism)</term>
<term>Phosphotransferases (Alcohol Group Acceptor) (genetics)</term>
<term>Phosphotransferases (Alcohol Group Acceptor) (metabolism)</term>
<term>Phytophthora infestans (metabolism)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Seedlings (MeSH)</term>
<term>Solanum tuberosum (metabolism)</term>
<term>Solanum tuberosum (microbiology)</term>
<term>Tobacco (metabolism)</term>
<term>Tobacco (microbiology)</term>
<term>Two-Hybrid System Techniques (MeSH)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Agrobacterium (métabolisme)</term>
<term>Animaux (MeSH)</term>
<term>Chloroplastes (microbiologie)</term>
<term>Chloroplastes (métabolisme)</term>
<term>Escherichia coli (métabolisme)</term>
<term>Extinction de l'expression des gènes (MeSH)</term>
<term>Lumière (MeSH)</term>
<term>Microscopie confocale (MeSH)</term>
<term>Phosphotransferases (Alcohol Group Acceptor) (génétique)</term>
<term>Phosphotransferases (Alcohol Group Acceptor) (métabolisme)</term>
<term>Phytophthora infestans (métabolisme)</term>
<term>Plant (MeSH)</term>
<term>Protéines NLR (génétique)</term>
<term>Protéines NLR (métabolisme)</term>
<term>Protéines fongiques (MeSH)</term>
<term>Protéines végétales (génétique)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Régulation de l'expression des gènes codant pour des enzymes (MeSH)</term>
<term>Régulation de l'expression des gènes végétaux (effets des radiations)</term>
<term>Régulation de l'expression des gènes végétaux (immunologie)</term>
<term>Solanum tuberosum (microbiologie)</term>
<term>Solanum tuberosum (métabolisme)</term>
<term>Tabac (microbiologie)</term>
<term>Tabac (métabolisme)</term>
<term>Techniques de double hybride (MeSH)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>NLR Proteins</term>
<term>Phosphotransferases (Alcohol Group Acceptor)</term>
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>NLR Proteins</term>
<term>Phosphotransferases (Alcohol Group Acceptor)</term>
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" xml:lang="en">
<term>Fungal Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="effets des radiations" xml:lang="fr">
<term>Régulation de l'expression des gènes végétaux</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Phosphotransferases (Alcohol Group Acceptor)</term>
<term>Protéines NLR</term>
<term>Protéines végétales</term>
</keywords>
<keywords scheme="MESH" qualifier="immunologie" xml:lang="fr">
<term>Régulation de l'expression des gènes végétaux</term>
</keywords>
<keywords scheme="MESH" qualifier="immunology" xml:lang="en">
<term>Gene Expression Regulation, Plant</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Agrobacterium</term>
<term>Chloroplasts</term>
<term>Escherichia coli</term>
<term>Phytophthora infestans</term>
<term>Solanum tuberosum</term>
<term>Tobacco</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Chloroplastes</term>
<term>Solanum tuberosum</term>
<term>Tabac</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Chloroplasts</term>
<term>Solanum tuberosum</term>
<term>Tobacco</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Agrobacterium</term>
<term>Chloroplastes</term>
<term>Escherichia coli</term>
<term>Phosphotransferases (Alcohol Group Acceptor)</term>
<term>Phytophthora infestans</term>
<term>Protéines NLR</term>
<term>Protéines végétales</term>
<term>Solanum tuberosum</term>
<term>Tabac</term>
</keywords>
<keywords scheme="MESH" qualifier="radiation effects" xml:lang="en">
<term>Gene Expression Regulation, Plant</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Animals</term>
<term>Gene Expression Regulation, Enzymologic</term>
<term>Gene Silencing</term>
<term>Light</term>
<term>Microscopy, Confocal</term>
<term>Seedlings</term>
<term>Two-Hybrid System Techniques</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Animaux</term>
<term>Extinction de l'expression des gènes</term>
<term>Lumière</term>
<term>Microscopie confocale</term>
<term>Plant</term>
<term>Protéines fongiques</term>
<term>Régulation de l'expression des gènes codant pour des enzymes</term>
<term>Techniques de double hybride</term>
</keywords>
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<front>
<div type="abstract" xml:lang="en">In plants and animals, nucleotide-binding leucine-rich repeat (NLR) proteins are intracellular immune sensors that recognize and eliminate a wide range of invading pathogens. NLR-mediated immunity is known to be modulated by environmental factors. However, how pathogen recognition by NLRs is influenced by environmental factors such as light remains unclear. Here, we show that the agronomically important NLR Rpi-vnt1.1 requires light to confer disease resistance against races of the Irish potato famine pathogen
<i>Phytophthora infestans</i>
that secrete the effector protein AVRvnt1. The activation of Rpi-vnt1.1 requires a nuclear-encoded chloroplast protein, glycerate 3-kinase (GLYK), implicated in energy production. The pathogen effector AVRvnt1 binds the full-length chloroplast-targeted GLYK isoform leading to activation of Rpi-vnt1.1. In the dark, Rpi-vnt1.1-mediated resistance is compromised because plants produce a shorter GLYK-lacking the intact chloroplast transit peptide-that is not bound by AVRvnt1. The transition between full-length and shorter plant GLYK transcripts is controlled by a light-dependent alternative promoter selection mechanism. In plants that lack Rpi-vnt1.1, the presence of AVRvnt1 reduces GLYK accumulation in chloroplasts counteracting GLYK contribution to basal immunity. Our findings revealed that pathogen manipulation of chloroplast functions has resulted in a light-dependent immune response.</div>
</front>
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<Day>10</Day>
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<Issue>17</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>Pathogen manipulation of chloroplast function triggers a light-dependent immune recognition.</ArticleTitle>
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<AbstractText>In plants and animals, nucleotide-binding leucine-rich repeat (NLR) proteins are intracellular immune sensors that recognize and eliminate a wide range of invading pathogens. NLR-mediated immunity is known to be modulated by environmental factors. However, how pathogen recognition by NLRs is influenced by environmental factors such as light remains unclear. Here, we show that the agronomically important NLR Rpi-vnt1.1 requires light to confer disease resistance against races of the Irish potato famine pathogen
<i>Phytophthora infestans</i>
that secrete the effector protein AVRvnt1. The activation of Rpi-vnt1.1 requires a nuclear-encoded chloroplast protein, glycerate 3-kinase (GLYK), implicated in energy production. The pathogen effector AVRvnt1 binds the full-length chloroplast-targeted GLYK isoform leading to activation of Rpi-vnt1.1. In the dark, Rpi-vnt1.1-mediated resistance is compromised because plants produce a shorter GLYK-lacking the intact chloroplast transit peptide-that is not bound by AVRvnt1. The transition between full-length and shorter plant GLYK transcripts is controlled by a light-dependent alternative promoter selection mechanism. In plants that lack Rpi-vnt1.1, the presence of AVRvnt1 reduces GLYK accumulation in chloroplasts counteracting GLYK contribution to basal immunity. Our findings revealed that pathogen manipulation of chloroplast functions has resulted in a light-dependent immune response.</AbstractText>
<CopyrightInformation>Copyright © 2020 the Author(s). Published by PNAS.</CopyrightInformation>
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<LastName>Gao</LastName>
<ForeName>Chuyun</ForeName>
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<Affiliation>College of Plant Protection, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
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<LastName>Yan</LastName>
<ForeName>Tingxiu</ForeName>
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<AffiliationInfo>
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</AffiliationInfo>
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<Author ValidYN="Y">
<LastName>Wang</LastName>
<ForeName>Yuanchao</ForeName>
<Initials>Y</Initials>
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<Affiliation>College of Plant Protection, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
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<AffiliationInfo>
<Affiliation>Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
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<Identifier Source="ORCID">0000-0002-8160-4556</Identifier>
<AffiliationInfo>
<Affiliation>Wageningen University and Research Plant Breeding, Wageningen University and Research, Wageningen 6708 PB, The Netherlands.</Affiliation>
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<LastName>Kamoun</LastName>
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<Affiliation>Imperial College, South Kensington Campus, SW7 2AZ London, United Kingdom.</Affiliation>
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<LastName>Dong</LastName>
<ForeName>Suomeng</ForeName>
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<Identifier Source="ORCID">0000-0002-9623-6776</Identifier>
<AffiliationInfo>
<Affiliation>College of Plant Protection, Nanjing Agricultural University, 210095 Nanjing, China; smdong@njau.edu.cn.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>The Sainsbury Laboratory, University of East Anglia, NR4 7UH Norwich, United Kingdom.</Affiliation>
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<AffiliationInfo>
<Affiliation>Key Laboratory of Plant Immunity, Nanjing Agricultural University, 210095 Nanjing, China.</Affiliation>
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<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
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<DescriptorName UI="D011198" MajorTopicYN="N">Solanum tuberosum</DescriptorName>
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<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
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<MeshHeading>
<DescriptorName UI="D014026" MajorTopicYN="N">Tobacco</DescriptorName>
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<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
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<Keyword MajorTopicYN="Y">potato blight</Keyword>
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<CoiStatement>Competing interest statement: S.K. filed a patent on NLR applications (WO/2019/108619A1).</CoiStatement>
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<Citation>Plant Cell. 2012 Aug;24(8):3420-34</Citation>
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