title: Folivory elicits a strong defense reaction in Catharanthus roseus: metabolomic and transcriptomic analyses reveal distinct local and systemic responses.
abstract: Plants deploy distinct secondary metabolisms to cope with environment pressure and to face bio-aggressors notably through the production of biologically active alkaloids. This metabolism-type is particularly elaborated in Catharanthus roseus that synthesizes more than a hundred different monoterpene indole alkaloids (MIAs). While the characterization of their biosynthetic pathway now reaches completion, still little is known about the role of MIAs during biotic attacks. As a consequence, we developed a new plant/herbivore interaction system by challenging C. roseus leaves with Manduca sexta larvae. Transcriptomic and metabolic analyses demonstrated that C. roseus respond to folivory by both local and systemic processes relying on the activation of specific gene sets and biosynthesis of distinct MIAs following jasmonate production. While a huge local accumulation of strictosidine was monitored in attacked leaves that could repel caterpillars through its protein reticulation properties, newly developed leaves displayed an increased biosynthesis of the toxic strictosidine-derived MIAs, vindoline and catharanthine, produced by up-regulation of MIA biosynthetic genes. In this context, leaf consumption resulted in a rapid death of caterpillars that could be linked to the MIA dimerization observed in intestinal tracts. Furthermore, this study also highlights the overall transcriptomic control of the plant defense processes occurring during herbivory.
authors.affiliation: Université François-Rabelais de Tours, EA2106 "Biomolécules et Biotechnologies Végétales", Tours, France.
authors.forename: Thomas
authors.initials: T
authors.lastname: Dugé de Bernonville
authors.affiliation: Université François-Rabelais de Tours, EA2106 "Biomolécules et Biotechnologies Végétales", Tours, France.
authors.forename: Inês
authors.initials: I
authors.lastname: Carqueijeiro
authors.affiliation: Université François-Rabelais de Tours, EA2106 "Biomolécules et Biotechnologies Végétales", Tours, France.
authors.forename: Arnaud
authors.initials: A
authors.lastname: Lanoue
authors.affiliation: Université François-Rabelais de Tours, EA2106 "Biomolécules et Biotechnologies Végétales", Tours, France.
authors.forename: Florent
authors.initials: F
authors.lastname: Lafontaine
authors.affiliation: Metabolic Integration and Cell Signaling Group, Plant Physiology Section, Department of CAMN, Universitat Jaume I, Spain.
authors.forename: Paloma
authors.initials: P
authors.lastname: Sánchez Bel
authors.affiliation: Université François-Rabelais de Tours, EA2106 "Biomolécules et Biotechnologies Végétales", Tours, France.
authors.forename: Franziska
authors.initials: F
authors.lastname: Liesecke
authors.affiliation: Institut de Recherche sur la Biologie de l'Insecte, UMR 7261, CNRS/Université François-Rabelais de Tours, Tours, France.
authors.forename: Karine
authors.initials: K
authors.lastname: Musset
authors.affiliation: Université François-Rabelais de Tours, EA2106 "Biomolécules et Biotechnologies Végétales", Tours, France.
authors.forename: Audrey
authors.initials: A
authors.lastname: Oudin
authors.affiliation: Université François-Rabelais de Tours, EA2106 "Biomolécules et Biotechnologies Végétales", Tours, France.
authors.forename: Gaëlle
authors.initials: G
authors.lastname: Glévarec
authors.affiliation: Université François-Rabelais de Tours, EA2106 "Biomolécules et Biotechnologies Végétales", Tours, France.
authors.forename: Olivier
authors.initials: O
authors.lastname: Pichon
authors.affiliation: Université François-Rabelais de Tours, EA2106 "Biomolécules et Biotechnologies Végétales", Tours, France.
authors.forename: Sébastien
authors.initials: S
authors.lastname: Besseau
authors.affiliation: Université François-Rabelais de Tours, EA2106 "Biomolécules et Biotechnologies Végétales", Tours, France.
authors.forename: Marc
authors.initials: M
authors.lastname: Clastre
authors.affiliation: Université François-Rabelais de Tours, EA2106 "Biomolécules et Biotechnologies Végétales", Tours, France.
authors.forename: Benoit
authors.initials: B
authors.lastname: St-Pierre
authors.affiliation: Metabolic Integration and Cell Signaling Group, Plant Physiology Section, Department of CAMN, Universitat Jaume I, Spain.
authors.forename: Victor
authors.initials: V
authors.lastname: Flors
authors.affiliation: Université d'Orléans, CoST, Laboratoire de Biologie des Ligneux et des Grandes Cultures (LBLGC), EA 1207, USC1328 INRA, Orléans, France.
authors.forename: Stéphane
authors.initials: S
authors.lastname: Maury
authors.affiliation: Institut de Recherche sur la Biologie de l'Insecte, UMR 7261, CNRS/Université François-Rabelais de Tours, Tours, France.
authors.forename: Elisabeth
authors.initials: E
authors.lastname: Huguet
authors.affiliation: The John Innes Centre, Department of Biological Chemistry, Norwich NR4 7UH, United Kingdom.
authors.forename: Sarah E
authors.initials: SE
authors.lastname: O'Connor
authors.affiliation: Université François-Rabelais de Tours, EA2106 "Biomolécules et Biotechnologies Végétales", Tours, France.
authors.forename: Vincent
authors.initials: V
authors.lastname: Courdavault
mesh_terms: D000818:Animals; D053898:Biosynthetic Pathways / Q000235:genetics; D030008:Catharanthus / Q000235:genetics / Q000276:immunology* / Q000378:metabolism*; D003517:Cyclopentanes / Q000378:metabolism; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant; D060434:Herbivory / Q000502:physiology*; D026121:Indole Alkaloids / Q000737:chemistry / Q000378:metabolism; D007814:Larva / Q000502:physiology; D018402:Manduca / Q000502:physiology; D055432:Metabolomics; D008954:Models, Biological; D039821:Monoterpenes / Q000737:chemistry / Q000378:metabolism; D054883:Oxylipins / Q000378:metabolism; D010788:Photosynthesis; D018515:Plant Leaves / Q000235:genetics* / Q000378:metabolism*; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D014158:Transcription, Genetic
chemical_list: D003517:Cyclopentanes; D026121:Indole Alkaloids; D039821:Monoterpenes; D054883:Oxylipins; D010940:Plant Proteins; D012333:RNA, Messenger; C011006:jasmonic acid