The Poplar Rust-Induced Secreted Protein (RISP) Inhibits the Growth of the Leaf Rust Pathogen Melampsora larici-populina and Triggers Cell Culture Alkalinisation.
Identifieur interne : 001639 ( Main/Exploration ); précédent : 001638; suivant : 001640The Poplar Rust-Induced Secreted Protein (RISP) Inhibits the Growth of the Leaf Rust Pathogen Melampsora larici-populina and Triggers Cell Culture Alkalinisation.
Auteurs : Benjamin Petre [Royaume-Uni] ; Arnaud Hecker [France] ; Hugo Germain [Canada] ; Pascale Tsan [France] ; Jan Sklenar [Royaume-Uni] ; Gervais Pelletier [Canada] ; Armand Séguin [Canada] ; Sébastien Duplessis [France] ; Nicolas Rouhier [France]Source :
- Frontiers in plant science [ 1664-462X ] ; 2016.
Abstract
Plant cells secrete a wide range of proteins in extracellular spaces in response to pathogen attack. The poplar rust-induced secreted protein (RISP) is a small cationic protein of unknown function that was identified as the most induced gene in poplar leaves during immune responses to the leaf rust pathogen Melampsora larici-populina, an obligate biotrophic parasite. Here, we combined in planta and in vitro molecular biology approaches to tackle the function of RISP. Using a RISP-mCherry fusion transiently expressed in Nicotiana benthamiana leaves, we demonstrated that RISP is secreted into the apoplast. A recombinant RISP specifically binds to M. larici-populina urediniospores and inhibits their germination. It also arrests the growth of the fungus in vitro and on poplar leaves. Interestingly, RISP also triggers poplar cell culture alkalinisation and is cleaved at the C-terminus by a plant-encoded mechanism. Altogether our results indicate that RISP is an antifungal protein that has the ability to trigger cellular responses.
DOI: 10.3389/fpls.2016.00097
PubMed: 26925067
PubMed Central: PMC4756128
Affiliations:
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Faculté des Sciences et Technologies, UMR 1136 Interactions Arbres/Microorganismes, Université de LorraineVandoeuvre-lès-Nancy, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Recherche Agronomique, Centre INRA Nancy Lorraine, UMR 1136 Interactions Arbres/MicroorganismesChampenoux, France; Faculté des Sciences et Technologies, UMR 1136 Interactions Arbres/Microorganismes, Université de LorraineVandoeuvre-lès-Nancy</wicri:regionArea><wicri:noRegion>Université de LorraineVandoeuvre-lès-Nancy</wicri:noRegion><wicri:noRegion>Université de LorraineVandoeuvre-lès-Nancy</wicri:noRegion></affiliation></author><author><name sortKey="Rouhier, Nicolas" sort="Rouhier, Nicolas" uniqKey="Rouhier N" first="Nicolas" last="Rouhier">Nicolas Rouhier</name><affiliation wicri:level="1"><nlm:affiliation>Institut National de la Recherche Agronomique, Centre INRA Nancy Lorraine, UMR 1136 Interactions Arbres/MicroorganismesChampenoux, France; Faculté des Sciences et Technologies, UMR 1136 Interactions Arbres/Microorganismes, Université de LorraineVandoeuvre-lès-Nancy, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Recherche Agronomique, Centre INRA Nancy Lorraine, UMR 1136 Interactions Arbres/MicroorganismesChampenoux, France; 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Faculté des Sciences et Technologies, UMR 1136 Interactions Arbres/Microorganismes, Université de LorraineVandoeuvre-lès-Nancy, France; The Sainsbury LaboratoryNorwich, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Institut National de la Recherche Agronomique, Centre INRA Nancy Lorraine, UMR 1136 Interactions Arbres/MicroorganismesChampenoux, France; Faculté des Sciences et Technologies, UMR 1136 Interactions Arbres/Microorganismes, Université de LorraineVandoeuvre-lès-Nancy, France; The Sainsbury LaboratoryNorwich</wicri:regionArea><wicri:noRegion>France; The Sainsbury LaboratoryNorwich</wicri:noRegion></affiliation></author><author><name sortKey="Hecker, Arnaud" sort="Hecker, Arnaud" uniqKey="Hecker A" first="Arnaud" last="Hecker">Arnaud Hecker</name><affiliation wicri:level="1"><nlm:affiliation>Institut National de la Recherche Agronomique, Centre INRA Nancy Lorraine, UMR 1136 Interactions Arbres/MicroorganismesChampenoux, France; Faculté des Sciences et Technologies, UMR 1136 Interactions Arbres/Microorganismes, Université de LorraineVandoeuvre-lès-Nancy, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Recherche Agronomique, Centre INRA Nancy Lorraine, UMR 1136 Interactions Arbres/MicroorganismesChampenoux, France; Faculté des Sciences et Technologies, UMR 1136 Interactions Arbres/Microorganismes, Université de LorraineVandoeuvre-lès-Nancy</wicri:regionArea><wicri:noRegion>Université de LorraineVandoeuvre-lès-Nancy</wicri:noRegion><wicri:noRegion>Université de LorraineVandoeuvre-lès-Nancy</wicri:noRegion></affiliation></author><author><name sortKey="Germain, Hugo" sort="Germain, Hugo" uniqKey="Germain H" first="Hugo" last="Germain">Hugo Germain</name><affiliation wicri:level="4"><nlm:affiliation>Groupe de Recherche en Biologie Végétale, Université du Québec à Trois-Rivières, Trois-Rivières QC, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Groupe de Recherche en Biologie Végétale, Université du Québec à Trois-Rivières, Trois-Rivières QC</wicri:regionArea><orgName type="university">Université du Québec à Trois-Rivières</orgName><placeName><settlement type="city">Trois-Rivières</settlement><region type="state">Québec</region></placeName></affiliation></author><author><name sortKey="Tsan, Pascale" sort="Tsan, Pascale" uniqKey="Tsan P" first="Pascale" last="Tsan">Pascale Tsan</name><affiliation wicri:level="1"><nlm:affiliation>CRM2, Equipe BioMod, Faculté des Sciences et Technologies, UMR 7036, Université de LorraineVandoeuvre-lès-Nancy, France; CNRS, CRM2, Equipe BioMod, Faculté des Sciences et Technologies, UMR 7036Vandoeuvre-lès-Nancy, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>CRM2, Equipe BioMod, Faculté des Sciences et Technologies, UMR 7036, Université de LorraineVandoeuvre-lès-Nancy, France; CNRS, CRM2, Equipe BioMod, Faculté des Sciences et Technologies, UMR 7036Vandoeuvre-lès-Nancy</wicri:regionArea><wicri:noRegion>UMR 7036Vandoeuvre-lès-Nancy</wicri:noRegion><wicri:noRegion>UMR 7036Vandoeuvre-lès-Nancy</wicri:noRegion></affiliation></author><author><name sortKey="Sklenar, Jan" sort="Sklenar, Jan" uniqKey="Sklenar J" first="Jan" last="Sklenar">Jan Sklenar</name><affiliation wicri:level="1"><nlm:affiliation>The Sainsbury Laboratory Norwich, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>The Sainsbury Laboratory Norwich</wicri:regionArea></affiliation></author><author><name sortKey="Pelletier, Gervais" sort="Pelletier, Gervais" uniqKey="Pelletier G" first="Gervais" last="Pelletier">Gervais Pelletier</name><affiliation wicri:level="1"><nlm:affiliation>Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Québec QC, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Québec QC</wicri:regionArea><wicri:noRegion>Québec QC</wicri:noRegion></affiliation></author><author><name sortKey="Seguin, Armand" sort="Seguin, Armand" uniqKey="Seguin A" first="Armand" last="Séguin">Armand Séguin</name><affiliation wicri:level="1"><nlm:affiliation>Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Québec QC, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Québec QC</wicri:regionArea><wicri:noRegion>Québec QC</wicri:noRegion></affiliation></author><author><name sortKey="Duplessis, Sebastien" sort="Duplessis, Sebastien" uniqKey="Duplessis S" first="Sébastien" last="Duplessis">Sébastien Duplessis</name><affiliation wicri:level="1"><nlm:affiliation>Institut National de la Recherche Agronomique, Centre INRA Nancy Lorraine, UMR 1136 Interactions Arbres/MicroorganismesChampenoux, France; Faculté des Sciences et Technologies, UMR 1136 Interactions Arbres/Microorganismes, Université de LorraineVandoeuvre-lès-Nancy, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Recherche Agronomique, Centre INRA Nancy Lorraine, UMR 1136 Interactions Arbres/MicroorganismesChampenoux, France; Faculté des Sciences et Technologies, UMR 1136 Interactions Arbres/Microorganismes, Université de LorraineVandoeuvre-lès-Nancy</wicri:regionArea><wicri:noRegion>Université de LorraineVandoeuvre-lès-Nancy</wicri:noRegion><wicri:noRegion>Université de LorraineVandoeuvre-lès-Nancy</wicri:noRegion></affiliation></author><author><name sortKey="Rouhier, Nicolas" sort="Rouhier, Nicolas" uniqKey="Rouhier N" first="Nicolas" last="Rouhier">Nicolas Rouhier</name><affiliation wicri:level="1"><nlm:affiliation>Institut National de la Recherche Agronomique, Centre INRA Nancy Lorraine, UMR 1136 Interactions Arbres/MicroorganismesChampenoux, France; Faculté des Sciences et Technologies, UMR 1136 Interactions Arbres/Microorganismes, Université de LorraineVandoeuvre-lès-Nancy, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Recherche Agronomique, Centre INRA Nancy Lorraine, UMR 1136 Interactions Arbres/MicroorganismesChampenoux, France; Faculté des Sciences et Technologies, UMR 1136 Interactions Arbres/Microorganismes, Université de LorraineVandoeuvre-lès-Nancy</wicri:regionArea><wicri:noRegion>Université de LorraineVandoeuvre-lès-Nancy</wicri:noRegion><wicri:noRegion>Université de LorraineVandoeuvre-lès-Nancy</wicri:noRegion></affiliation></author></analytic><series><title level="j">Frontiers in plant science</title><idno type="ISSN">1664-462X</idno><imprint><date when="2016" type="published">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Plant cells secrete a wide range of proteins in extracellular spaces in response to pathogen attack. The poplar rust-induced secreted protein (RISP) is a small cationic protein of unknown function that was identified as the most induced gene in poplar leaves during immune responses to the leaf rust pathogen Melampsora larici-populina, an obligate biotrophic parasite. Here, we combined in planta and in vitro molecular biology approaches to tackle the function of RISP. Using a RISP-mCherry fusion transiently expressed in Nicotiana benthamiana leaves, we demonstrated that RISP is secreted into the apoplast. A recombinant RISP specifically binds to M. larici-populina urediniospores and inhibits their germination. It also arrests the growth of the fungus in vitro and on poplar leaves. Interestingly, RISP also triggers poplar cell culture alkalinisation and is cleaved at the C-terminus by a plant-encoded mechanism. Altogether our results indicate that RISP is an antifungal protein that has the ability to trigger cellular responses. </div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">26925067</PMID><DateCompleted><Year>2016</Year><Month>02</Month><Day>29</Day></DateCompleted><DateRevised><Year>2020</Year><Month>09</Month><Day>29</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-462X</ISSN><JournalIssue CitedMedium="Print"><Volume>7</Volume><PubDate><Year>2016</Year></PubDate></JournalIssue><Title>Frontiers in plant science</Title><ISOAbbreviation>Front Plant Sci</ISOAbbreviation></Journal><ArticleTitle>The Poplar Rust-Induced Secreted Protein (RISP) Inhibits the Growth of the Leaf Rust Pathogen Melampsora larici-populina and Triggers Cell Culture Alkalinisation.</ArticleTitle><Pagination><MedlinePgn>97</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fpls.2016.00097</ELocationID><Abstract><AbstractText>Plant cells secrete a wide range of proteins in extracellular spaces in response to pathogen attack. The poplar rust-induced secreted protein (RISP) is a small cationic protein of unknown function that was identified as the most induced gene in poplar leaves during immune responses to the leaf rust pathogen Melampsora larici-populina, an obligate biotrophic parasite. Here, we combined in planta and in vitro molecular biology approaches to tackle the function of RISP. Using a RISP-mCherry fusion transiently expressed in Nicotiana benthamiana leaves, we demonstrated that RISP is secreted into the apoplast. A recombinant RISP specifically binds to M. larici-populina urediniospores and inhibits their germination. It also arrests the growth of the fungus in vitro and on poplar leaves. Interestingly, RISP also triggers poplar cell culture alkalinisation and is cleaved at the C-terminus by a plant-encoded mechanism. Altogether our results indicate that RISP is an antifungal protein that has the ability to trigger cellular responses. </AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Petre</LastName><ForeName>Benjamin</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Institut National de la Recherche Agronomique, Centre INRA Nancy Lorraine, UMR 1136 Interactions Arbres/MicroorganismesChampenoux, France; Faculté des Sciences et Technologies, UMR 1136 Interactions Arbres/Microorganismes, Université de LorraineVandoeuvre-lès-Nancy, France; The Sainsbury LaboratoryNorwich, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hecker</LastName><ForeName>Arnaud</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Institut National de la Recherche Agronomique, Centre INRA Nancy Lorraine, UMR 1136 Interactions Arbres/MicroorganismesChampenoux, France; Faculté des Sciences et Technologies, UMR 1136 Interactions Arbres/Microorganismes, Université de LorraineVandoeuvre-lès-Nancy, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Germain</LastName><ForeName>Hugo</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Groupe de Recherche en Biologie Végétale, Université du Québec à Trois-Rivières, Trois-Rivières QC, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tsan</LastName><ForeName>Pascale</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>CRM2, Equipe BioMod, Faculté des Sciences et Technologies, UMR 7036, Université de LorraineVandoeuvre-lès-Nancy, France; CNRS, CRM2, Equipe BioMod, Faculté des Sciences et Technologies, UMR 7036Vandoeuvre-lès-Nancy, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sklenar</LastName><ForeName>Jan</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>The Sainsbury Laboratory Norwich, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pelletier</LastName><ForeName>Gervais</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Québec QC, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Séguin</LastName><ForeName>Armand</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Québec QC, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Duplessis</LastName><ForeName>Sébastien</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Institut National de la Recherche Agronomique, Centre INRA Nancy Lorraine, UMR 1136 Interactions Arbres/MicroorganismesChampenoux, France; Faculté des Sciences et Technologies, UMR 1136 Interactions Arbres/Microorganismes, Université de LorraineVandoeuvre-lès-Nancy, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rouhier</LastName><ForeName>Nicolas</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Institut National de la Recherche Agronomique, Centre INRA Nancy Lorraine, UMR 1136 Interactions Arbres/MicroorganismesChampenoux, France; Faculté des Sciences et Technologies, UMR 1136 Interactions Arbres/Microorganismes, Université de LorraineVandoeuvre-lès-Nancy, France.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2016</Year><Month>02</Month><Day>17</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Plant Sci</MedlineTA><NlmUniqueID>101568200</NlmUniqueID><ISSNLinking>1664-462X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Populus trichocarpa</Keyword><Keyword MajorTopicYN="N">antifungal activity</Keyword><Keyword MajorTopicYN="N">obligate biotroph</Keyword><Keyword MajorTopicYN="N">peptide elicitor</Keyword><Keyword MajorTopicYN="N">plant immunity</Keyword><Keyword MajorTopicYN="N">rust fungus</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2015</Year><Month>11</Month><Day>11</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2016</Year><Month>01</Month><Day>18</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2016</Year><Month>3</Month><Day>1</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2016</Year><Month>3</Month><Day>1</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2016</Year><Month>3</Month><Day>1</Day><Hour>6</Hour><Minute>1</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">26925067</ArticleId><ArticleId 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