Sclareol and linalyl acetate are produced by glandular trichomes through the MEP pathway

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Abstract

Sclareol, an antifungal specialized metabolite produced by clary sage, Salvia sclarea, is the starting plant natural molecule used for the hemisynthesis of the perfume ingredient ambroxide. Sclareol is mainly produced in clary sage flower calyces; however, the cellular localization of the sclareol biosynthesis remains unknown. To elucidate the site of sclareol biosynthesis, we analyzed its spatial distribution in the clary sage calyx epidermis using laser desorption/ionization mass spectrometry imaging (LDI–FTICR-MSI) and investigated the expression profile of sclareol biosynthesis genes in isolated glandular trichomes (GTs). We showed that sclareol specifically accumulates in GTs’ gland cells in which sclareol biosynthesis genes are strongly expressed. We next isolated a glabrous beardless mutant and demonstrate that more than 90% of the sclareol is produced by the large capitate GTs. Feeding experiments, using 1- ¹³C-glucose, and specific enzyme inhibitors further revealed that the methylerythritol-phosphate (MEP) biosynthetic pathway is the main source of isopentenyl diphosphate (IPP) precursor used for the biosynthesis of sclareol. Our findings demonstrate that sclareol is an MEP-derived diterpene produced by large capitate GTs in clary sage emphasing the role of GTs as biofactories dedicated to the production of specialized metabolites.

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Terpenoids (isoprenoids) represent the largest and most diverse class of chemicals among the myriad compounds produced by plants. Plants employ terpenoid metabolites for a variety of basic functions in growth and development but use the majority of terpenoids for more specialized chemical interactions and protection in the abiotic and biotic environment. Traditionally, plant-based terpenoids have been used by humans in the food, pharmaceutical, and chemical industries, and more recently have been exploited in the development of biofuel products. Genomic resources and emerging tools in synthetic biology facilitate the metabolic engineering of high-value terpenoid products in plants and microbes. Moreover, the ecological importance of terpenoids has gained increased attention to develop strategies for sustainable pest control and abiotic stress protection. Together, these efforts require a continuous growth in knowledge of the complex metabolic and molecular regulatory networks in terpenoid biosynthesis. This chapter gives an overview and highlights recent advances in our understanding of the organization, regulation, and diversification of core and specialized terpenoid metabolic pathways, and addresses the most important functions of volatile and nonvolatile terpenoid specialized metabolites in plants.

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Author and article information

Contributors

Adnane Boualem: adnane.boualem@inrae.fr

Journal

Journal ID (nlm-ta): Hortic Res

Journal ID (iso-abbrev): Hortic Res

Title: Horticulture Research

Publisher: Nature Publishing Group UK (London )

ISSN (Print): 2662-6810

ISSN (Electronic): 2052-7276

Publication date (Electronic): 1 October 2021

Publication date PMC-release: 1 October 2021

Publication date Collection: 2021

Volume: 8

Electronic Location Identifier: 206

Affiliations

[1 ]Université Paris-Saclay, CNRS, INRAE, Univ Evry, Institute of Plant Sciences Paris-Saclay (IPS2), 91405 Orsay, France

[2 ]GRID grid.4444.0, ISNI 0000 0001 2112 9282, Molecular Chemistry Laboratory (LCM), UMR 9168, CNRS, Ecole Polytechnique, Institut Polytechnique de Paris, Route de Saclay, ; 91128 Palaiseau Cedex, France

[3 ]GRID grid.460789.4, ISNI 0000 0004 4910 6535, Laboratory of Mechanics of Soils, Structures and Materials (MSSMAT), UMR 8579, CNRS, Ecole CentraleSupélec, Université Paris-Saclay, Bâtiment Eiffel, 8-10 rue Joliot-Curie, ; 91190 Gif-Sur-Yvette, France

Author information

Françoise Gilard http://orcid.org/0000-0001-9314-1555

Article

Publisher ID: 640

DOI: 10.1038/s41438-021-00640-w

PMC ID: 8484277

PubMed ID: 34593779

SO-VID: 3855a1cb-3922-4f8e-801d-67719a43dbe1

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 10 April 2021

Date revision received : 9 July 2021

Date accepted : 22 July 2021

Funding

Funded by: FundRef https://doi.org/10.13039/501100001665, Agence Nationale de la Recherche (French National Research Agency);

Award ID: ANR-10-LABX-40-SPS

Award Recipient : Camille Chalvin Françoise Gilard Caroline Mauve Christel Chollet Halima Morin Lucie Kriegshauser Bertrand Gakière Abdelhafid Bendahmane Adnane Boualem

Funded by: INRAE Plant Biology and Breeding department French NAtional FT-ICR network

Funded by: funder: National FT-ICR network grant number FR 3624 CNRS