A cytosolic bifunctional geranyl/farnesyl diphosphate synthase provides MVA-derived GPP for geraniol biosynthesis in rose flowers
2023
Conart, Corentin | Bomzan, Dikki Pedenla | Huang, Xing-Qi | Bassard, Jean-Etienne | Paramita, Saretta N. | Saint-Marcoux, Denis | Rius-Bony, Aurélie | Hivert, Gal | Anchisi, Anthony | Schaller, Hubert | Hamama, Latifa | Magnard, Jean-Louis | Lipko, Agata | Swiezewska, Ewa | Jame, Patrick | Riveill, Geneviève | Hibrand-Saint Oyant, Laurence | Rohmer, Michel | Lewinsohn, Efraim | Dudareva, Natalia | Baudino, Sylvie | Caissard, Jean-Claude | Boachon, Benoit | Laboratoire de Biotechnologies Végétales appliquées aux Plantes Aromatiques et Médicinales (BVPAM) ; Université Jean Monnet - Saint-Étienne (UJM)-Centre National de la Recherche Scientifique (CNRS) | Purdue University [West Lafayette] | Institut de Biologie Moléculaire des Plantes (IBMP) ; Université de Strasbourg (UNISTRA)-Centre National de la Recherche Scientifique (CNRS) | The Hebrew University of Jerusalem (HUJ) | Institut des Sciences Analytiques (ISA) ; Université Claude Bernard Lyon 1 (UCBL) ; Université de Lyon-Université de Lyon-Institut de Chimie - CNRS Chimie (INC-CNRS)-Centre National de la Recherche Scientifique (CNRS) | ISA-Isotopique & Organique - Isotopic & Organic ; Institut des Sciences Analytiques (ISA) ; Université Claude Bernard Lyon 1 (UCBL) ; Université de Lyon-Université de Lyon-Institut de Chimie - CNRS Chimie (INC-CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL) ; Université de Lyon-Université de Lyon-Institut de Chimie - CNRS Chimie (INC-CNRS)-Centre National de la Recherche Scientifique (CNRS) | Institut de Recherche en Horticulture et Semences (IRHS) ; Université d'Angers (UA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut Agro Rennes Angers ; Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro) | Nalecz Institute of Biocybernetics and Biomedical Engineering (IBIB) | Institute of Biochemistry and Biophysics [Warsaw] (IBB) | Santé de la vigne et qualité du vin (SVQV) ; Université de Strasbourg (UNISTRA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) | Institut de Chimie de Strasbourg (IC) ; Université de Strasbourg (UNISTRA)-Institut de Chimie - CNRS Chimie (INC-CNRS)-Centre National de la Recherche Scientifique (CNRS) | Indiana University - Purdue University Indianapolis (IUPUI) ; Indiana University System | The National Science Foundation IOS-1655438 and by the USDA National Institute of Food and Agriculture Hatch Project number 177845 to N.D. | ANR-16-CE20-0024,ROSASCENT,Biosynthèse des terpènes du parfum chez la rose(2016)
International audience
Show more [+] Less [-]English. Geraniol derived from essential oils of various plant species is widely used in the cosmetic and perfume industries. It is also an essential trait of the pleasant smell of rose flowers. In contrast to other monoterpenes which are produced in plastids via the methyl erythritol phosphate pathway, geraniol biosynthesis in roses relies on cytosolic NUDX1 hydrolase which dephosphorylates geranyl diphosphate (GPP). However, the metabolic origin of cytosolic GPP remains unknown. By feeding Rosa chinensis “Old Blush” flowers with pathway-specific precursors and inhibitors, combined with metabolic profiling and functional characterization of enzymes in vitro and in planta, we show that geraniol is synthesized through the cytosolic mevalonate (MVA) pathway by a bifunctional geranyl/farnesyl diphosphate synthase, RcG/FPPS1, producing both GPP and farnesyl diphosphate (FPP). The downregulation and overexpression of RcG/FPPS1 in rose petals affected not only geraniol and germacrene D emissions but also dihydro-β-ionol, the latter due to metabolic cross talk of RcG/FPPS1-dependent isoprenoid intermediates trafficking from the cytosol to plastids. Phylogenetic analysis together with functional characterization of G/FPPS orthologs revealed that the G/FPPS activity is conserved among Rosaceae species. Site-directed mutagenesis and molecular dynamic simulations enabled to identify two conserved amino acids that evolved from ancestral FPPSs and contribute to GPP/FPP product specificity. Overall, this study elucidates the origin of the cytosolic GPP for NUDX1-dependent geraniol production, provides insights into the emergence of the RcG/FPPS1 GPPS activity from the ancestral FPPSs, and shows that RcG/FPPS1 plays a key role in the biosynthesis of volatile terpenoid compounds in rose flowers.
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