Extracellular Localization of the Diterpene Sclareol in Clary Sage (Salvia sclarea L., Lamiaceae)

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Abstract

Sclareol is a high-value natural product obtained by solid/liquid extraction of clary sage ( Salvia sclarea L.) inflorescences. Because processes of excretion and accumulation of this labdane diterpene are unknown, the aim of this work was to gain knowledge on its sites of accumulation in planta. Samples were collected in natura or during different steps of the industrial process of extraction (steam distillation and solid/liquid extraction). Samples were then analysed with a combination of complementary analytical techniques (gas chromatography coupled to a mass spectrometer, polarized light microscopy, environmental scanning electron microscopy, two-photon fluorescence microscopy, second harmonic generation microscopy). According to the literature, it is hypothesized that sclareol is localized in oil pockets of secretory trichomes. This study demonstrates that this is not the case and that sclareol accumulates in a crystalline epicuticular form, mostly on calyces.

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Sealing plant surfaces: cuticular wax formation by epidermal cells.

Lacey Samuels, Ljerka Kunst, Reinhard Jetter (2008)

The vital importance of plant surface wax in protecting tissue from environmental stresses is reflected in the huge commitment of epidermal cells to cuticle formation. During cuticle deposition, a massive flux of lipids occurs from the sites of lipid synthesis in the plastid and the endoplasmic reticulum to the plant surface. Recent genetic studies in Arabidopsis have improved our understanding of fatty acid elongation and of the subsequent modification of the elongated products into primary alcohols, wax esters, secondary alcohols, and ketones, shedding light on the enzymes involved in these pathways. In contrast, the biosynthesis of alkanes is still poorly understood, as are the mechanisms of wax transport from the site of biosynthesis to the cuticle. Currently, nothing is known about wax trafficking from the endoplasmic reticulum to the plasma membrane, or about translocation through the cell wall to the cuticle. However, a first breakthrough toward an understanding of wax export recently came with the discovery of ATP binding cassette (ABC) transporters that are involved in releasing wax from the plasma membrane into the apoplast. An overview of our present knowledge of wax biosynthesis and transport and the regulation of these processes during cuticle assembly is presented, including the evidence for coordination of cutin polyester and wax production.

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Biosynthesis and secretion of plant cuticular wax.

Benjamin A. Samuels, L Kunst (2002)

The cuticle covers the aerial portions of land plants. It consists of amorphous intracuticular wax embedded in cutin polymer, and epicuticular wax crystalloids that coat the outer plant surface and impart a whitish appearance. Cuticular wax is mainly composed of long-chain aliphatic compounds derived from very long chain fatty acids. Wax biosynthesis begins with fatty acid synthesis in the plastid. Here we focus on fatty acid elongation (FAE) to very long chains (C24-C34), and the subsequent processing of these elongated products into alkanes, secondary alcohols, ketones, primary alcohols and wax esters. The identity of the gene products involved in these processes is starting to emerge. Other areas of this field remain enigmatic. For example, it is not known how the hydrophobic wax components are moved intracellularly, how they are exported out of the cell, or translocated through the hydrophilic cell wall. Two hypotheses are presented for intracellular wax transport: direct transfer of lipids from the endoplasmic reticulum to the plasma membrane, and Golgi mediated exocytosis. The potential roles of ABC transporters and non-specific lipid transfer proteins in wax export are also discussed. Biochemical-genetic and genomic approaches in Arabidopsis thaliana promise to be particularly useful in identifying and characterizing gene products involved in wax biosynthesis, secretion and function. The current review will, therefore, focus on Arabidopsis as a model for studying these processes.

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A plant plasma membrane ATP binding cassette-type transporter is involved in antifungal terpenoid secretion.

Y Stukkens, H Degand, Jean Jasinski … (2001)

ATP binding cassette (ABC) transporters, which are found in all species, are known mainly for their ability to confer drug resistance. To date, most of the ABC transporters characterized in plants have been localized in the vacuolar membrane and are considered to be involved in the intracellular sequestration of cytotoxins. Working on the assumption that certain ABC transporters might be involved in defense metabolite secretion and their expression might be regulated by the concentration of these metabolites, we treated a Nicotiana plumbaginifolia cell culture with sclareolide, a close analog of sclareol, an antifungal diterpene produced at the leaf surface of Nicotiana spp; this resulted in the appearance of a 160-kD plasma membrane protein, which was partially sequenced. The corresponding cDNA (NpABC1) was cloned and shown to encode an ABC transporter. In vitro and in situ immunodetection showed NpABC1 to be localized in the plasma membrane. Under normal conditions, expression was found in the leaf epidermis. In cell culture and in leaf tissues, NpABC1 expression was strongly enhanced by sclareolide and sclareol. In parallel with NpABC1 induction, cells acquired the ability to excrete a labeled synthetic sclareolide derivative. These data suggest that NpABC1 is involved in the secretion of a secondary metabolite that plays a role in plant defense.

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Author and article information

Contributors

Joshua L. Heazlewood: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, USA )

ISSN (Electronic): 1932-6203

Publication date Collection: 2012

Publication date (Electronic): 25 October 2012

Volume: 7

Issue: 10

Electronic Location Identifier: e48253

Affiliations

[1 ]Laboratoire de Biotechnologies Végétales Appliquées aux Plantes Aromatiques et Médicinales, Université Jean Monnet, Université de Lyon, Saint-Etienne, France

[2 ]Laboratoire Hubert Curien, Université Jean Monnet, Université de Lyon, Saint-Etienne, France

[3 ]Bontoux S.A., Saint-Auban-sur-Ouvèze, France

[4 ]Centre de Microscopie Confocale Multiphotonique, Université Jean Monnet, Université de Lyon, Saint-Etienne, France

[5 ]Laboratoire Stress Abiotiques et Différenciation des Végétaux Cultivés, Université Lille Nord de France, Université Lille 1, Villeneuve d'Ascq, France

Lawrence Berkeley National Laboratory, United States of America

Author notes

* E-mail: caissard@ 123456univ-st-etienne.fr

Competing Interests: CD, AA and PPG are employees of Bontoux SA. There are no patents, products in development or marketed products to declare. This does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials.

Conceived and designed the experiments: JCC TO FJ PPG. Performed the experiments: JCC TO SP FJ AA SL. Analyzed the data: JCC TO FN SB. Contributed reagents/materials/analysis tools: NV SM FN JLM SL CD AA SP. Wrote the paper: JCC TO SB FJ CD. Industrial extractions: CD PPG AA. Sampling authorizations in grower fields: PPG AA.

Article

Publisher ID: PONE-D-12-20306

DOI: 10.1371/journal.pone.0048253

PMC ID: 3484996

PubMed ID: 23133579

SO-VID: 154a0efb-1008-42d3-88ed-1b29ce9068a8

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 11 July 2012

Date accepted : 21 September 2012

Page count

Pages: 8

Funding

This work is part of the Claryssime Programme ( http://www.claryssime.fr/) supervised by CD, and including a PostDoc grant to SL. Claryssime is funded by “Pôle de Compétitivité Parfums, Arômes, Senteurs, Saveurs”, “Direction Générale de la Compétitivité, de l’Industrie et des Services” and “Région Rhône-Alpes”. Laser microscopy is funded by Université Jean Monnet, CNRS and Leica Microsystem. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Extracellular Localization of the Diterpene Sclareol in Clary Sage ( Salvia sclarea L., Lamiaceae)

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Most cited references 25

Sealing plant surfaces: cuticular wax formation by epidermal cells.

Biosynthesis and secretion of plant cuticular wax.

A plant plasma membrane ATP binding cassette-type transporter is involved in antifungal terpenoid secretion.

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