title: Leaf-mining by Phyllonorycter blancardella reprograms the host-leaf transcriptome to modulate phytohormones associated with nutrient mobilization and plant defense.
abstract: Phytohormones have long been hypothesized to play a key role in the interactions between plant-manipulating organisms and their host-plants such as insect-plant interactions that lead to gall or 'green-islands' induction. However, mechanistic understanding of how phytohormones operate in these plant reconfigurations is lacking due to limited information on the molecular and biochemical phytohormonal modulation following attack by plant-manipulating insects. In an attempt to fill this gap, the present study provides an extensive characterization of how the leaf-miner Phyllonorycter blancardella modulates the major phytohormones and the transcriptional activity of plant cells in leaves of Malus domestica. We show here, that cytokinins strongly accumulate in mined tissues despite a weak expression of plant cytokinin-related genes. Leaf-mining is also associated with enhanced biosynthesis of jasmonic acid precursors but not the active form, a weak alteration of the salicylic acid pathway and a clear inhibition of the abscisic acid pathway. Our study consolidates previous results suggesting that insects may produce and deliver cytokinins to the plant as a strategy to manipulate the physiology of the leaf to create a favorable nutritional environment. We also demonstrate that leaf-mining by P. blancardella leads to a strong reprogramming of the plant phytohormonal balance associated with increased nutrient mobilization, inhibition of leaf senescence and mitigation of plant direct and indirect defense.
authors.affiliation: Institut de Recherche sur la Biologie de l'Insecte, UMR 7261, CNRS/Université François-Rabelais de Tours, Tours, France. Electronic address: hui.zhang@etu.univ-tours.fr.
authors.forename: Hui
authors.initials: H
authors.lastname: Zhang
authors.affiliation: Laboratoire Biologie Végétale et Biomolécules, EA 2106, Université François-Rabelais de Tours, Tours, France. Electronic address: thomas.duge@univ-tours.fr.
authors.forename: Thomas
authors.initials: T
authors.lastname: Dugé de Bernonville
authors.affiliation: Institut de Recherche sur la Biologie de l'Insecte, UMR 7261, CNRS/Université François-Rabelais de Tours, Tours, France. Electronic address: bodym@missouri.edu.
authors.forename: Mélanie
authors.initials: M
authors.lastname: Body
authors.affiliation: Laboratoire Biologie Végétale et Biomolécules, EA 2106, Université François-Rabelais de Tours, Tours, France. Electronic address: gaelle.glevarec@univ-tours.fr.
authors.forename: Gaëlle
authors.initials: G
authors.lastname: Glevarec
authors.affiliation: Department of Biochemistry, Max-Planck-Institute for Chemical Ecology, Jena, Germany. Electronic address: reichelt@ice.mpg.de.
authors.forename: Michael
authors.initials: M
authors.lastname: Reichelt
authors.affiliation: Department of Biochemistry, Max-Planck-Institute for Chemical Ecology, Jena, Germany. Electronic address: sunsicker@ice.mpg.de.
authors.forename: Sybille
authors.initials: S
authors.lastname: Unsicker
authors.affiliation: Institut de Recherche en Horticulture et Semences, UMR 1345, INRA, SFR 4207 QuaSaV, Beaucouzé, France. Electronic address: maryline.bruneau@angers.inra.fr.
authors.forename: Maryline
authors.initials: M
authors.lastname: Bruneau
authors.affiliation: Institut de Recherche en Horticulture et Semences, UMR 1345, INRA, SFR 4207 QuaSaV, Beaucouzé, France. Electronic address: jean-pierre.renou@angers.inra.fr.
authors.forename: Jean-Pierre
authors.initials: JP
authors.lastname: Renou
authors.affiliation: Institut de Recherche sur la Biologie de l'Insecte, UMR 7261, CNRS/Université François-Rabelais de Tours, Tours, France. Electronic address: elisabeth.huguet@univ-tours.fr.
authors.forename: Elisabeth
authors.initials: E
authors.lastname: Huguet
authors.affiliation: Institut de Recherche sur la Biologie de l'Insecte, UMR 7261, CNRS/Université François-Rabelais de Tours, Tours, France. Electronic address: geraldine.dubreuil@univ-tours.fr.
authors.forename: Géraldine
authors.initials: G
authors.lastname: Dubreuil
authors.affiliation: Institut de Recherche sur la Biologie de l'Insecte, UMR 7261, CNRS/Université François-Rabelais de Tours, Tours, France. Electronic address: david.giron@univ-tours.fr.
authors.forename: David
authors.initials: D
authors.lastname: Giron
mesh_terms: D000818:Animals; D006790:Host-Parasite Interactions; D007915:Lepidoptera / Q000502:physiology*; D027845:Malus / Q000469:parasitology*; D010937:Plant Growth Regulators / Q000378:metabolism*; D057865:Plant Immunity; D018515:Plant Leaves / Q000378:metabolism / Q000469:parasitology*; D059467:Transcriptome
chemical_list: D010937:Plant Growth Regulators
keywords: Cytokinins; Insects; Leaf-mining; Phytohormones