Inducible biosynthesis and immune function of the systemic acquired resistance inducer N-hydroxypipecolic acid in monocotyledonous and dicotyledonous plants.
Identifieur interne : 000149 ( Main/Exploration ); précédent : 000148; suivant : 000150Inducible biosynthesis and immune function of the systemic acquired resistance inducer N-hydroxypipecolic acid in monocotyledonous and dicotyledonous plants.
Auteurs : Anika Schnake [Allemagne] ; Michael Hartmann [Allemagne] ; Stefan Schreiber [Allemagne] ; Jana Malik [Allemagne] ; Lisa Brahmann [Allemagne] ; Ipek Yildiz [Allemagne] ; Janina Von Dahlen [Allemagne] ; Laura E. Rose [Allemagne] ; Ulrich Schaffrath [Allemagne] ; Jürgen Zeier [Allemagne]Source :
- Journal of experimental botany [ 1460-2431 ] ; 2020.
Abstract
Recent work has provided evidence for the occurrence of N-hydroxypipecolic acid (NHP) in Arabidopsis thaliana, characterized its pathogen-inducible biosynthesis by a three-step metabolic sequence from l-lysine, and established a central role for NHP in the regulation of systemic acquired resistance. Here, we show that NHP is biosynthesized in several other plant species in response to microbial attack, generally together with its direct metabolic precursor pipecolic acid and the phenolic immune signal salicylic acid. For example, NHP accumulates locally in inoculated leaves and systemically in distant leaves of cucumber in response to Pseudomonas syringae attack, in Pseudomonas-challenged tobacco and soybean leaves, in tomato inoculated with the oomycete Phytophthora infestans, in leaves of the monocot Brachypodium distachyon infected with bacterial (Xanthomonas translucens) and fungal (Magnaporthe oryzae) pathogens, and in M. oryzae-inoculated barley. Notably, resistance assays indicate that NHP acts as a potent inducer of acquired resistance to bacterial and fungal infection in distinct monocotyledonous and dicotyledonous species. Pronounced systemic accumulation of NHP in leaf phloem sap of locally inoculated cucumber supports a function for NHP as a phloem-mobile immune signal. Our study thus generalizes the existence and function of an NHP resistance pathway in plant systemic acquired resistance.
DOI: 10.1093/jxb/eraa317
PubMed: 32725118
PubMed Central: PMC7586749
Affiliations:
- Allemagne
- District de Cologne, District de Düsseldorf, Rhénanie-du-Nord-Westphalie
- Aix-la-Chapelle, Düsseldorf
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sort="Von Dahlen, Janina" uniqKey="Von Dahlen J" first="Janina" last="Von Dahlen">Janina Von Dahlen</name><affiliation wicri:level="3"><nlm:affiliation>Institute for Population Genetics, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Population Genetics, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Düsseldorf</region><settlement type="city">Düsseldorf</settlement></placeName></affiliation></author><author><name sortKey="Rose, Laura E" sort="Rose, Laura E" uniqKey="Rose L" first="Laura E" last="Rose">Laura E. 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N-hydroxypipecolic acid in monocotyledonous and dicotyledonous plants.</title><author><name sortKey="Schnake, Anika" sort="Schnake, Anika" uniqKey="Schnake A" first="Anika" last="Schnake">Anika Schnake</name><affiliation wicri:level="3"><nlm:affiliation>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Düsseldorf</region><settlement type="city">Düsseldorf</settlement></placeName></affiliation></author><author><name sortKey="Hartmann, Michael" sort="Hartmann, Michael" uniqKey="Hartmann M" first="Michael" last="Hartmann">Michael Hartmann</name><affiliation wicri:level="3"><nlm:affiliation>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Düsseldorf</region><settlement type="city">Düsseldorf</settlement></placeName></affiliation></author><author><name sortKey="Schreiber, Stefan" sort="Schreiber, Stefan" uniqKey="Schreiber S" first="Stefan" last="Schreiber">Stefan Schreiber</name><affiliation wicri:level="3"><nlm:affiliation>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Düsseldorf</region><settlement type="city">Düsseldorf</settlement></placeName></affiliation></author><author><name sortKey="Malik, Jana" sort="Malik, Jana" uniqKey="Malik J" first="Jana" last="Malik">Jana Malik</name><affiliation wicri:level="3"><nlm:affiliation>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Düsseldorf</region><settlement type="city">Düsseldorf</settlement></placeName></affiliation></author><author><name sortKey="Brahmann, Lisa" sort="Brahmann, Lisa" uniqKey="Brahmann L" first="Lisa" last="Brahmann">Lisa Brahmann</name><affiliation wicri:level="3"><nlm:affiliation>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Düsseldorf</region><settlement type="city">Düsseldorf</settlement></placeName></affiliation></author><author><name sortKey="Yildiz, Ipek" sort="Yildiz, Ipek" uniqKey="Yildiz I" first="Ipek" last="Yildiz">Ipek Yildiz</name><affiliation wicri:level="3"><nlm:affiliation>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Düsseldorf</region><settlement type="city">Düsseldorf</settlement></placeName></affiliation></author><author><name sortKey="Von Dahlen, Janina" sort="Von Dahlen, Janina" uniqKey="Von Dahlen J" first="Janina" last="Von Dahlen">Janina Von Dahlen</name><affiliation wicri:level="3"><nlm:affiliation>Institute for Population Genetics, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Population Genetics, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Düsseldorf</region><settlement type="city">Düsseldorf</settlement></placeName></affiliation></author><author><name sortKey="Rose, Laura E" sort="Rose, Laura E" uniqKey="Rose L" first="Laura E" last="Rose">Laura E. Rose</name><affiliation wicri:level="3"><nlm:affiliation>Institute for Population Genetics, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Population Genetics, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Düsseldorf</region><settlement type="city">Düsseldorf</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich Heine University, Universitätsstraße 1, Düsseldorf</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Düsseldorf</region><settlement type="city">Düsseldorf</settlement></placeName></affiliation></author><author><name sortKey="Schaffrath, Ulrich" sort="Schaffrath, Ulrich" uniqKey="Schaffrath U" first="Ulrich" last="Schaffrath">Ulrich Schaffrath</name><affiliation wicri:level="3"><nlm:affiliation>Department of Plant Physiology, RWTH Aachen University, Aachen, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Plant Physiology, RWTH Aachen University, Aachen</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Aix-la-Chapelle</settlement></placeName></affiliation></author><author><name sortKey="Zeier, Jurgen" sort="Zeier, Jurgen" uniqKey="Zeier J" first="Jürgen" last="Zeier">Jürgen Zeier</name><affiliation wicri:level="3"><nlm:affiliation>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Düsseldorf</region><settlement type="city">Düsseldorf</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich Heine University, Universitätsstraße 1, Düsseldorf</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Düsseldorf</region><settlement type="city">Düsseldorf</settlement></placeName></affiliation></author></analytic><series><title level="j">Journal of experimental botany</title><idno type="eISSN">1460-2431</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Recent work has provided evidence for the occurrence of N-hydroxypipecolic acid (NHP) in Arabidopsis thaliana, characterized its pathogen-inducible biosynthesis by a three-step metabolic sequence from l-lysine, and established a central role for NHP in the regulation of systemic acquired resistance. Here, we show that NHP is biosynthesized in several other plant species in response to microbial attack, generally together with its direct metabolic precursor pipecolic acid and the phenolic immune signal salicylic acid. For example, NHP accumulates locally in inoculated leaves and systemically in distant leaves of cucumber in response to Pseudomonas syringae attack, in Pseudomonas-challenged tobacco and soybean leaves, in tomato inoculated with the oomycete Phytophthora infestans, in leaves of the monocot Brachypodium distachyon infected with bacterial (Xanthomonas translucens) and fungal (Magnaporthe oryzae) pathogens, and in M. oryzae-inoculated barley. Notably, resistance assays indicate that NHP acts as a potent inducer of acquired resistance to bacterial and fungal infection in distinct monocotyledonous and dicotyledonous species. Pronounced systemic accumulation of NHP in leaf phloem sap of locally inoculated cucumber supports a function for NHP as a phloem-mobile immune signal. Our study thus generalizes the existence and function of an NHP resistance pathway in plant systemic acquired resistance.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">32725118</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>31</Day></DateRevised><Article PubModel="Print"><Journal><ISSN IssnType="Electronic">1460-2431</ISSN><JournalIssue CitedMedium="Internet"><Volume>71</Volume><Issue>20</Issue><PubDate><Year>2020</Year><Month>Oct</Month><Day>22</Day></PubDate></JournalIssue><Title>Journal of experimental botany</Title><ISOAbbreviation>J Exp Bot</ISOAbbreviation></Journal><ArticleTitle>Inducible biosynthesis and immune function of the systemic acquired resistance inducer N-hydroxypipecolic acid in monocotyledonous and dicotyledonous plants.</ArticleTitle><Pagination><MedlinePgn>6444-6459</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1093/jxb/eraa317</ELocationID><Abstract><AbstractText>Recent work has provided evidence for the occurrence of N-hydroxypipecolic acid (NHP) in Arabidopsis thaliana, characterized its pathogen-inducible biosynthesis by a three-step metabolic sequence from l-lysine, and established a central role for NHP in the regulation of systemic acquired resistance. Here, we show that NHP is biosynthesized in several other plant species in response to microbial attack, generally together with its direct metabolic precursor pipecolic acid and the phenolic immune signal salicylic acid. For example, NHP accumulates locally in inoculated leaves and systemically in distant leaves of cucumber in response to Pseudomonas syringae attack, in Pseudomonas-challenged tobacco and soybean leaves, in tomato inoculated with the oomycete Phytophthora infestans, in leaves of the monocot Brachypodium distachyon infected with bacterial (Xanthomonas translucens) and fungal (Magnaporthe oryzae) pathogens, and in M. oryzae-inoculated barley. Notably, resistance assays indicate that NHP acts as a potent inducer of acquired resistance to bacterial and fungal infection in distinct monocotyledonous and dicotyledonous species. Pronounced systemic accumulation of NHP in leaf phloem sap of locally inoculated cucumber supports a function for NHP as a phloem-mobile immune signal. Our study thus generalizes the existence and function of an NHP resistance pathway in plant systemic acquired resistance.</AbstractText><CopyrightInformation>© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Experimental Biology.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Schnake</LastName><ForeName>Anika</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hartmann</LastName><ForeName>Michael</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schreiber</LastName><ForeName>Stefan</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Malik</LastName><ForeName>Jana</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Brahmann</LastName><ForeName>Lisa</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yildiz</LastName><ForeName>Ipek</ForeName><Initials>I</Initials><AffiliationInfo><Affiliation>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>von Dahlen</LastName><ForeName>Janina</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Institute for Population Genetics, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rose</LastName><ForeName>Laura E</ForeName><Initials>LE</Initials><AffiliationInfo><Affiliation>Institute for Population Genetics, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schaffrath</LastName><ForeName>Ulrich</ForeName><Initials>U</Initials><AffiliationInfo><Affiliation>Department of Plant Physiology, RWTH Aachen University, Aachen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zeier</LastName><ForeName>Jürgen</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Institute for Molecular Ecophysiology of Plants, Department of Biology, Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich Heine University, Universitätsstraße 1, Düsseldorf, Germany.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>J Exp Bot</MedlineTA><NlmUniqueID>9882906</NlmUniqueID><ISSNLinking>0022-0957</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Brachypodium
</Keyword><Keyword MajorTopicYN="N">Magnaporthe
</Keyword><Keyword MajorTopicYN="N">N-hydroxypipecolic acid</Keyword><Keyword MajorTopicYN="N">Pseudomonas
</Keyword><Keyword MajorTopicYN="N">cucumber</Keyword><Keyword MajorTopicYN="N">pipecolic acid</Keyword><Keyword MajorTopicYN="N">plant immunity</Keyword><Keyword MajorTopicYN="N">salicylic acid</Keyword><Keyword MajorTopicYN="N">systemic acquired resistance</Keyword><Keyword MajorTopicYN="N">tobacco</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>04</Month><Day>07</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>07</Month><Day>02</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>7</Month><Day>30</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>7</Month><Day>30</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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