Salivary proteins of Phloeomyzus passerinii, a plant-manipulating aphid, and their impact on early gene responses of susceptible and resistant poplar genotypes.
Identifieur interne : 000369 ( Main/Curation ); précédent : 000368; suivant : 000370Salivary proteins of Phloeomyzus passerinii, a plant-manipulating aphid, and their impact on early gene responses of susceptible and resistant poplar genotypes.
Auteurs : Luis Portillo Lemus [France] ; Jessy Tricard [France] ; Jérôme Duclercq [France] ; Quentin Coulette [France] ; David Giron [France] ; Christophe Hano [France] ; Elisabeth Huguet [France] ; Frédéric Lamblin [France] ; Anas Cherqui [France] ; Aurélien Sallé [France]Source :
- Plant science : an international journal of experimental plant biology [ 1873-2259 ] ; 2020.
Abstract
Successful plant colonization by parasites requires the circumvention of host defenses, and sometimes a reprogramming of host metabolism, mediated by effector molecules delivered into the host. Using transcriptomic and enzymatic approaches, we characterized salivary glands and saliva of Phloeomyzus passerinii, an aphid exhibiting an atypical feeding strategy. Plant responses to salivary extracts of P. passerinii and Myzus persicae were assessed with poplar protoplasts of a susceptible and a resistant genotype, and in a heterologous Arabidopsis system. We predict that P. passerinii secretes a highly peculiar saliva containing effectors potentially interfering with host defenses, biotic stress signaling and plant metabolism, notably phosphatidylinositol phosphate kinases which seemed specific to P. passerinii. Gene expression profiles indicated that salivary extracts of M. persicae markedly affected host defenses and biotic stress signaling, while salivary extracts of P. passerinii induced only weak responses. The effector-triggered susceptibility was characterized by downregulations of genes involved in cytokinin signaling and auxin homeostasis. This suggests that P. passerinii induces an intracellular accumulation of auxin in susceptible host genotypes, which is supported by histochemical assays in Arabidopsis. This might in turn affect biotic stress signaling and contribute to host tissue manipulation by the aphid.
DOI: 10.1016/j.plantsci.2020.110468
PubMed: 32234233
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Ecologie et Dynamique des Systèmes Anthropisés, EDYSAN UMR CNRS-UPJV 7058, Université de Picardie Jules Verne, Amiens, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire de Biologie des Ligneux et des Grandes Cultures, INRA, Université d'Orléans, 45067, Orléans, France; Ecologie et Dynamique des Systèmes Anthropisés, EDYSAN UMR CNRS-UPJV 7058, Université de Picardie Jules Verne, Amiens</wicri:regionArea></affiliation></author><author><name sortKey="Tricard, Jessy" sort="Tricard, Jessy" uniqKey="Tricard J" first="Jessy" last="Tricard">Jessy Tricard</name><affiliation wicri:level="1"><nlm:affiliation>Laboratoire de Biologie des Ligneux et des Grandes Cultures, INRA, Université d'Orléans, 45067, Orléans, France; Ecologie et Dynamique des Systèmes Anthropisés, EDYSAN UMR CNRS-UPJV 7058, Université de Picardie Jules Verne, Amiens, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire de Biologie des Ligneux et des Grandes Cultures, INRA, Université d'Orléans, 45067, Orléans, France; Ecologie et Dynamique des Systèmes Anthropisés, EDYSAN UMR CNRS-UPJV 7058, Université de Picardie Jules Verne, Amiens</wicri:regionArea></affiliation></author><author><name sortKey="Duclercq, Jerome" sort="Duclercq, Jerome" uniqKey="Duclercq J" first="Jérôme" last="Duclercq">Jérôme Duclercq</name><affiliation wicri:level="1"><nlm:affiliation>Ecologie et Dynamique des Systèmes Anthropisés, EDYSAN UMR CNRS-UPJV 7058, Université de Picardie Jules Verne, Amiens, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Ecologie et Dynamique des Systèmes Anthropisés, EDYSAN UMR CNRS-UPJV 7058, Université de Picardie Jules Verne, Amiens</wicri:regionArea></affiliation></author><author><name sortKey="Coulette, Quentin" sort="Coulette, Quentin" uniqKey="Coulette Q" first="Quentin" last="Coulette">Quentin Coulette</name><affiliation wicri:level="1"><nlm:affiliation>Ecologie et Dynamique des Systèmes Anthropisés, EDYSAN UMR CNRS-UPJV 7058, Université de Picardie Jules Verne, Amiens, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Ecologie et Dynamique des Systèmes Anthropisés, EDYSAN UMR CNRS-UPJV 7058, Université de Picardie Jules Verne, Amiens</wicri:regionArea></affiliation></author><author><name sortKey="Giron, David" sort="Giron, David" uniqKey="Giron D" first="David" last="Giron">David Giron</name><affiliation wicri:level="1"><nlm:affiliation>Institut de Recherche sur la Biologie de l'Insecte, UMR 7261, CNRS/Université François-Rabelais de Tours, Tours, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut de Recherche sur la Biologie de l'Insecte, UMR 7261, CNRS/Université François-Rabelais de Tours, Tours</wicri:regionArea></affiliation></author><author><name sortKey="Hano, Christophe" sort="Hano, Christophe" uniqKey="Hano C" first="Christophe" last="Hano">Christophe Hano</name><affiliation wicri:level="1"><nlm:affiliation>Laboratoire de Biologie des Ligneux et des Grandes Cultures, INRA, Université d'Orléans, 45067, Orléans, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire de Biologie des Ligneux et des Grandes Cultures, INRA, Université d'Orléans, 45067, Orléans</wicri:regionArea></affiliation></author><author><name sortKey="Huguet, Elisabeth" sort="Huguet, Elisabeth" uniqKey="Huguet E" first="Elisabeth" last="Huguet">Elisabeth Huguet</name><affiliation wicri:level="1"><nlm:affiliation>Institut de Recherche sur la Biologie de l'Insecte, UMR 7261, CNRS/Université François-Rabelais de Tours, Tours, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut de Recherche sur la Biologie de l'Insecte, UMR 7261, CNRS/Université François-Rabelais de Tours, Tours</wicri:regionArea></affiliation></author><author><name sortKey="Lamblin, Frederic" sort="Lamblin, Frederic" uniqKey="Lamblin F" first="Frédéric" last="Lamblin">Frédéric Lamblin</name><affiliation wicri:level="1"><nlm:affiliation>Laboratoire de Biologie des Ligneux et des Grandes Cultures, INRA, Université d'Orléans, 45067, Orléans, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire de Biologie des Ligneux et des Grandes Cultures, INRA, Université d'Orléans, 45067, Orléans</wicri:regionArea></affiliation></author><author><name sortKey="Cherqui, Anas" sort="Cherqui, Anas" uniqKey="Cherqui A" first="Anas" last="Cherqui">Anas Cherqui</name><affiliation wicri:level="1"><nlm:affiliation>Ecologie et Dynamique des Systèmes Anthropisés, EDYSAN UMR CNRS-UPJV 7058, Université de Picardie Jules Verne, Amiens, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Ecologie et Dynamique des Systèmes Anthropisés, EDYSAN UMR CNRS-UPJV 7058, Université de Picardie Jules Verne, Amiens</wicri:regionArea></affiliation></author><author><name sortKey="Salle, Aurelien" sort="Salle, Aurelien" uniqKey="Salle A" first="Aurélien" last="Sallé">Aurélien Sallé</name><affiliation wicri:level="1"><nlm:affiliation>Laboratoire de Biologie des Ligneux et des Grandes Cultures, INRA, Université d'Orléans, 45067, Orléans, France. Electronic address: aurelien.salle@univ-orleans.fr.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire de Biologie des Ligneux et des Grandes Cultures, INRA, Université d'Orléans, 45067, Orléans</wicri:regionArea></affiliation></author></analytic><series><title level="j">Plant science : an international journal of experimental plant biology</title><idno type="eISSN">1873-2259</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">Successful plant colonization by parasites requires the circumvention of host defenses, and sometimes a reprogramming of host metabolism, mediated by effector molecules delivered into the host. Using transcriptomic and enzymatic approaches, we characterized salivary glands and saliva of Phloeomyzus passerinii, an aphid exhibiting an atypical feeding strategy. Plant responses to salivary extracts of P. passerinii and Myzus persicae were assessed with poplar protoplasts of a susceptible and a resistant genotype, and in a heterologous Arabidopsis system. We predict that P. passerinii secretes a highly peculiar saliva containing effectors potentially interfering with host defenses, biotic stress signaling and plant metabolism, notably phosphatidylinositol phosphate kinases which seemed specific to P. passerinii. Gene expression profiles indicated that salivary extracts of M. persicae markedly affected host defenses and biotic stress signaling, while salivary extracts of P. passerinii induced only weak responses. The effector-triggered susceptibility was characterized by downregulations of genes involved in cytokinin signaling and auxin homeostasis. This suggests that P. passerinii induces an intracellular accumulation of auxin in susceptible host genotypes, which is supported by histochemical assays in Arabidopsis. This might in turn affect biotic stress signaling and contribute to host tissue manipulation by the aphid.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32234233</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>30</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1873-2259</ISSN><JournalIssue CitedMedium="Internet"><Volume>294</Volume><PubDate><Year>2020</Year><Month>May</Month></PubDate></JournalIssue><Title>Plant science : an international journal of experimental plant biology</Title><ISOAbbreviation>Plant Sci</ISOAbbreviation></Journal><ArticleTitle>Salivary proteins of Phloeomyzus passerinii, a plant-manipulating aphid, and their impact on early gene responses of susceptible and resistant poplar genotypes.</ArticleTitle><Pagination><MedlinePgn>110468</MedlinePgn></Pagination><ELocationID EIdType="pii" ValidYN="Y">S0168-9452(20)30070-4</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1016/j.plantsci.2020.110468</ELocationID><Abstract><AbstractText>Successful plant colonization by parasites requires the circumvention of host defenses, and sometimes a reprogramming of host metabolism, mediated by effector molecules delivered into the host. Using transcriptomic and enzymatic approaches, we characterized salivary glands and saliva of Phloeomyzus passerinii, an aphid exhibiting an atypical feeding strategy. Plant responses to salivary extracts of P. passerinii and Myzus persicae were assessed with poplar protoplasts of a susceptible and a resistant genotype, and in a heterologous Arabidopsis system. We predict that P. passerinii secretes a highly peculiar saliva containing effectors potentially interfering with host defenses, biotic stress signaling and plant metabolism, notably phosphatidylinositol phosphate kinases which seemed specific to P. passerinii. Gene expression profiles indicated that salivary extracts of M. persicae markedly affected host defenses and biotic stress signaling, while salivary extracts of P. passerinii induced only weak responses. The effector-triggered susceptibility was characterized by downregulations of genes involved in cytokinin signaling and auxin homeostasis. This suggests that P. passerinii induces an intracellular accumulation of auxin in susceptible host genotypes, which is supported by histochemical assays in Arabidopsis. This might in turn affect biotic stress signaling and contribute to host tissue manipulation by the aphid.</AbstractText><CopyrightInformation>Copyright © 2020 Elsevier B.V. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Portillo Lemus</LastName><ForeName>Luis</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Laboratoire de Biologie des Ligneux et des Grandes Cultures, INRA, Université d'Orléans, 45067, Orléans, France; Ecologie et Dynamique des Systèmes Anthropisés, EDYSAN UMR CNRS-UPJV 7058, Université de Picardie Jules Verne, Amiens, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tricard</LastName><ForeName>Jessy</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Laboratoire de Biologie des Ligneux et des Grandes Cultures, INRA, Université d'Orléans, 45067, Orléans, France; Ecologie et Dynamique des Systèmes Anthropisés, EDYSAN UMR CNRS-UPJV 7058, Université de Picardie Jules Verne, Amiens, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Duclercq</LastName><ForeName>Jérôme</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Ecologie et Dynamique des Systèmes Anthropisés, EDYSAN UMR CNRS-UPJV 7058, Université de Picardie Jules Verne, Amiens, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Coulette</LastName><ForeName>Quentin</ForeName><Initials>Q</Initials><AffiliationInfo><Affiliation>Ecologie et Dynamique des Systèmes Anthropisés, EDYSAN UMR CNRS-UPJV 7058, Université de Picardie Jules Verne, Amiens, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Giron</LastName><ForeName>David</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Institut de Recherche sur la Biologie de l'Insecte, UMR 7261, CNRS/Université François-Rabelais de Tours, Tours, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hano</LastName><ForeName>Christophe</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Laboratoire de Biologie des Ligneux et des Grandes Cultures, INRA, Université d'Orléans, 45067, Orléans, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Huguet</LastName><ForeName>Elisabeth</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>Institut de Recherche sur la Biologie de l'Insecte, UMR 7261, CNRS/Université François-Rabelais de Tours, Tours, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lamblin</LastName><ForeName>Frédéric</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Laboratoire de Biologie des Ligneux et des Grandes Cultures, INRA, Université d'Orléans, 45067, Orléans, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cherqui</LastName><ForeName>Anas</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Ecologie et Dynamique des Systèmes Anthropisés, EDYSAN UMR CNRS-UPJV 7058, Université de Picardie Jules Verne, Amiens, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sallé</LastName><ForeName>Aurélien</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Laboratoire de Biologie des Ligneux et des Grandes Cultures, INRA, Université d'Orléans, 45067, Orléans, France. Electronic address: aurelien.salle@univ-orleans.fr.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>03</Month><Day>12</Day></ArticleDate></Article><MedlineJournalInfo><Country>Ireland</Country><MedlineTA>Plant Sci</MedlineTA><NlmUniqueID>9882015</NlmUniqueID><ISSNLinking>0168-9452</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Auxin</Keyword><Keyword MajorTopicYN="N">Cytokinin</Keyword><Keyword MajorTopicYN="N">Effector</Keyword><Keyword MajorTopicYN="N">Effector-triggered susceptibility</Keyword><Keyword MajorTopicYN="N">Myzus persicae</Keyword><Keyword MajorTopicYN="N">Plant-insect interaction</Keyword><Keyword MajorTopicYN="N">Populus</Keyword><Keyword MajorTopicYN="N">Resistance</Keyword></KeywordList><CoiStatement>Declarations of Competing Interest None.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>08</Month><Day>30</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>03</Month><Day>03</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>03</Month><Day>10</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>4</Month><Day>3</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>4</Month><Day>3</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>4</Month><Day>3</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32234233</ArticleId><ArticleId IdType="pii">S0168-9452(20)30070-4</ArticleId><ArticleId IdType="doi">10.1016/j.plantsci.2020.110468</ArticleId></ArticleIdList></PubmedData></pubmed></record>Pour manipuler ce document sous Unix (Dilib)
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