title: CYP76C1 (Cytochrome P450)-Mediated Linalool Metabolism and the Formation of Volatile and Soluble Linalool Oxides in Arabidopsis Flowers: A Strategy for Defense against Floral Antagonists.
abstract: The acyclic monoterpene alcohol linalool is one of the most frequently encountered volatile compounds in floral scents. Various linalool oxides are usually emitted along with linalool, some of which are cyclic, such as the furanoid lilac compounds. Recent work has revealed the coexistence of two flower-expressed linalool synthases that produce the (S)- or (R)-linalool enantiomers and the involvement of two P450 enzymes in the linalool oxidation in the flowers of Arabidopsis thaliana. Partially redundant enzymes may also contribute to floral linalool metabolism. Here, we provide evidence that CYP76C1 is a multifunctional enzyme that catalyzes a cascade of oxidation reactions and is the major linalool metabolizing oxygenase in Arabidopsis flowers. Based on the activity of the recombinant enzyme and mutant analyses, we demonstrate its prominent role in the formation of most of the linalool oxides identified in vivo, both as volatiles and soluble conjugated compounds, including 8-hydroxy, 8-oxo, and 8-COOH-linalool, as well as lilac aldehydes and alcohols. Analysis of insect behavior on CYP76C1 mutants and in response to linalool and its oxygenated derivatives demonstrates that CYP76C1-dependent modulation of linalool emission and production of linalool oxides contribute to reduced floral attraction and favor protection against visitors and pests.
authors.affiliation: Institut de Biologie Moléculaire des Plantes du Centre National de la Recherche Scientifique (CNRS), Université de Strasbourg, 67000 Strasbourg, France.
authors.forename: Benoît
authors.identifier: http://orcid.org/0000-0002-2362-2238
authors.initials: B
authors.lastname: Boachon
authors.affiliation: Department of Ecology and Evolution, University of Salzburg, 5020 Slazburg, Austria.
authors.forename: Robert R
authors.identifier: http://orcid.org/0000-0002-7919-9678
authors.initials: RR
authors.lastname: Junker
authors.affiliation: Laboratoire de Chimie Organique Synthétique, Institut de Chimie, CNRS, Université de Strasbourg, 67000 Strasbourg, France.
authors.forename: Laurence
authors.identifier: http://orcid.org/0000-0002-0369-9908
authors.initials: L
authors.lastname: Miesch
authors.affiliation: VILLUM Research Center for Plant Plasticity, Center for Synthetic Biology "bioSYNergy," and Plant Biochemistry Laboratory, Department of Plant and Environmental Sciences, University of Copenhagen, DK-1871 Frederiksberg C, Copenhagen, Denmark.
authors.forename: Jean-Etienne
authors.identifier: http://orcid.org/0000-0002-7937-8027
authors.initials: JE
authors.lastname: Bassard
authors.affiliation: Institut de Biologie Moléculaire des Plantes du Centre National de la Recherche Scientifique (CNRS), Université de Strasbourg, 67000 Strasbourg, France.
authors.forename: René
authors.identifier: http://orcid.org/0000-0003-0964-1253
authors.initials: R
authors.lastname: Höfer
authors.affiliation: Institut de Biologie Moléculaire des Plantes du Centre National de la Recherche Scientifique (CNRS), Université de Strasbourg, 67000 Strasbourg, France.
authors.forename: Robin
authors.identifier: http://orcid.org/0000-0002-1255-7952
authors.initials: R
authors.lastname: Caillieaudeaux
authors.affiliation: Department of Ecology and Evolution, University of Salzburg, 5020 Slazburg, Austria.
authors.forename: Dana E
authors.identifier: http://orcid.org/0000-0002-8278-2346
authors.initials: DE
authors.lastname: Seidel
authors.affiliation: Institut de Biologie Moléculaire des Plantes du Centre National de la Recherche Scientifique (CNRS), Université de Strasbourg, 67000 Strasbourg, France.
authors.forename: Agnès
authors.initials: A
authors.lastname: Lesot
authors.affiliation: Laboratoire de Chimie Organique Synthétique, Institut de Chimie, CNRS, Université de Strasbourg, 67000 Strasbourg, France.
authors.forename: Clément
authors.identifier: http://orcid.org/0000-0003-0500-1734
authors.initials: C
authors.lastname: Heinrich
authors.affiliation: Institut de Biologie Moléculaire des Plantes du Centre National de la Recherche Scientifique (CNRS), Université de Strasbourg, 67000 Strasbourg, France.
authors.forename: Jean-François
authors.initials: JF
authors.lastname: Ginglinger
authors.affiliation: Plateforme d'Analyses pour la Chimie, CNRS, Université de Strasbourg, 67000 Strasbourg, France.
authors.forename: Lionel
authors.identifier: http://orcid.org/0000-0002-4766-3958
authors.initials: L
authors.lastname: Allouche
authors.affiliation: Plateforme d'Analyses pour la Chimie, CNRS, Université de Strasbourg, 67000 Strasbourg, France.
authors.forename: Bruno
authors.identifier: http://orcid.org/0000-0002-6415-2455
authors.initials: B
authors.lastname: Vincent
authors.affiliation: Institute of Biology, Plant Ecology, Leiden University, 2311E2 Leiden, The Netherlands.
authors.forename: Dinar S C
authors.identifier: http://orcid.org/0000-0002-4884-1672
authors.initials: DS
authors.lastname: Wahyuni
authors.affiliation: Max Planck Institute for Chemical Ecology, 07745 Jena, Germany.
authors.forename: Christian
authors.identifier: http://orcid.org/0000-0002-5776-7574
authors.initials: C
authors.lastname: Paetz
authors.affiliation: Max Planck Institute for Chemical Ecology, 07745 Jena, Germany.
authors.forename: Franziska
authors.initials: F
authors.lastname: Beran
authors.affiliation: Laboratoire de Chimie Organique Synthétique, Institut de Chimie, CNRS, Université de Strasbourg, 67000 Strasbourg, France.
authors.forename: Michel
authors.identifier: http://orcid.org/0000-0002-2633-8830
authors.initials: M
authors.lastname: Miesch
authors.affiliation: Max Planck Institute for Chemical Ecology, 07745 Jena, Germany.
authors.forename: Bernd
authors.initials: B
authors.lastname: Schneider
authors.affiliation: Institute of Biology, Plant Ecology, Leiden University, 2311E2 Leiden, The Netherlands.
authors.forename: Kirsten
authors.initials: K
authors.lastname: Leiss
authors.affiliation: Institut de Biologie Moléculaire des Plantes du Centre National de la Recherche Scientifique (CNRS), Université de Strasbourg, 67000 Strasbourg, France werck@unistra.fr.
authors.forename: Danièle
authors.initials: D
authors.lastname: Werck-Reichhart
mesh_terms: D000080462:Acyclic Monoterpenes; D000438:Alcohols / Q000737:chemistry / Q000378:metabolism; D000818:Animals; D017360:Arabidopsis / Q000201:enzymology* / Q000235:genetics / Q000276:immunology; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D003511:Cyclohexanols / Q000737:chemistry / Q000378:metabolism*; D003577:Cytochrome P-450 Enzyme System / Q000235:genetics / Q000378:metabolism*; D035264:Flowers / Q000201:enzymology* / Q000235:genetics / Q000276:immunology; D017930:Genes, Reporter; D007313:Insecta / Q000502:physiology; D007306:Insecticides / Q000737:chemistry / Q000378:metabolism*; D039821:Monoterpenes / Q000737:chemistry / Q000378:metabolism*; D010084:Oxidation-Reduction; D013237:Stereoisomerism; D014320:Triphenylmethyl Compounds / Q000737:chemistry / Q000378:metabolism*
chemical_list: D000080462:Acyclic Monoterpenes; D000438:Alcohols; D029681:Arabidopsis Proteins; D003511:Cyclohexanols; D007306:Insecticides; D039821:Monoterpenes; D014320:Triphenylmethyl Compounds; C000593345:linalool oxide; D003577:Cytochrome P-450 Enzyme System; C018584:linalool