ReviewThe chemical diversity and distribution of glucosinolates and isothiocyanates among plants☆
Introduction
The first observations on the unique properties of glucosinolates and isothiocyanates or mustard oils, as they are commonly known, were recorded at the beginning of the 17th century as a result of efforts to understand the chemical origin of the sharp taste of mustard seeds. The discovery and early history of glucosinolates and the participation of the enzyme myrosinase (a β-thioglucosidase) in their conversion to isothiocyanates, are the subjects of an interesting and scholarly review by Challenger (1959). The glucosinolates known by the trivial names sinigrin (2-propenyl or allyl glucosinolate; 1, Fig. 1) and sinalbin (4-hydroxybenzyl glucosinolate; 1, Fig. 1) were isolated early in the 1830s from black (Brassica nigra) and white (Sinapis alba) mustard seeds, respectively.2 (See Table 1, Table 2 for glucosinolate numbers used throughout this review.) The first general, although incorrect, structure for these compounds was proposed at the end of the nineteenth century by Gadamer (1897), who concluded that the side chain was linked to the nitrogen rather than the carbon atom of the “NCS” group. Despite certain difficulties the structure was generally assumed to be correct until 1956, when Ettlinger and Lundeen (1956a) pointed out the inadequacies of the Gadamer structure to explain certain properties of these compounds, proposed the now correct structure, and described the first chemical synthesis of a glucosinolate (Ettlinger and Lundeen, 1957). The remaining structural issue of the geometrical isomerism at the CN bond was established to be Z (or anti-) by X-ray crystallographic analysis of sinigrin (see Fig. 1; Marsh and Waser, 1970).
Glucosinolates are β-thioglucoside N-hydroxysulfates [also known as (Z)-(or cis)-N-hydroximinosulfate esters or S-glucopyranosyl thiohydroximates], with a side chain (R) and a sulfur-linked β-d-glucopyranose moiety.
In the last 40 years, a succession of reviews have addressed the biology and chemistry of glucosinolates (e.g. Kjær, 1961, Kjær, 1974; Ettlinger and Kjær, 1968, Kjær and Olesen Larsen, 1973, Kjær and Olesen Larsen, 1976; Underhill et al., 1973; Underhill, 1980; Fenwick et al., 1983; Chew, 1988; Duncan and Milne, 1989; Brown and Morra, 1997; Halkier, 1999; Mithen et al., 2000), and their distribution among plants (Rodman, 1981). More narrowly focused reviews have examined the indole glucosinolates (McDanell et al., 1988), or specifically glucosinolates in the family Brassicaceae (Kjær, 1976). Similar coverage (i.e. of glucosinolates of crop plants, primarily the Brassica vegetables) has been provided by Stoewsand (1995) and Rosa et al. (1997). Many other even more narrowly focused reviews have concentrated on specific plant families or on specific aspects of glucosinolate biology and they are referenced herein, as appropriate.
The present review provides a comprehensive survey of the chemical structures of all known glucosinolates and the plant families from which they have been isolated. It provides a single source of their chemical structure, their trivial names, and groups these compounds into families according to their structural similarities. We discuss, mostly by reference, the state of scientific understanding of the synthesis, biosynthesis and ecological importance of glucosinolates and their conversion to isothiocyanates and other products by myrosinase. To our knowledge, there has been no recent effort to provide a comprehensive compilation and cataloging of isolated glucosinolates, their structures, systematic and trivial (common) names, and their distribution among plant species. Although we have attempted to do so herein, undoubtedly there are omissions. Since many of these compounds were identified before modern spectroscopic techniques were available, some of the structural assignments of glucosinolates to plant taxa may require revision.
Section snippets
Glucosinolate distribution among plants
There is now a voluminous literature on the glucosinolates of the plant family, Brassicaceae, which alone contains more than 350 genera and 3000 species. Of the many hundreds of cruciferous species investigated, all are able to synthesize glucosinolates (Kjær, 1976). Among the Brassicaceae, the genus Brassica contains a large number of the commonly consumed species. Brassica sp. glucosinolates have been the subject of scholarly reviews by Kjær, 1974, Kjær, 1976), Fenwick et al. (1983), Chew
Types of glucosinolates
We have grouped glucosinolates into a number of chemical classes on the basis of structural similarities. The most extensively studied glucosinolates are the aliphatic, ω-methylthioalkyl, aromatic and heterocyclic (e.g. indole) glucosinolates, typified by those found in the Brassica vegetables (e.g. compounds 1, Fig. 1 in Table 1 and Fig. 1). Glucosinolate side chains, however, are characterized by a wide variety of chemical structures (Fig. 1). The most numerous glucosinolates are those
Hydrolysis of glucosinolates by plant and microbial myrosinases
Glucosinolates are very stable water-soluble precursors of isothiocyanates, and are typically present in fresh plants at much higher levels than their cognate isothiocyanates. Under carefully controlled conditions designed to extract glucosinolates and isothiocyanates completely, while preventing myrosinase activity, some fresh plants have been shown to contain almost exclusively glucosinolates (Fahey et al., 1997). The relatively nonreactive glucosinolates are converted to isothiocyanates upon
Glucosinolate content of plants
Glucosinolate content in plants is about 1% of dry weight in some tissues of the Brassica vegetables (Rosa et al., 1997), although the content is highly variable (Kushad et al., 1999, Farnham et al., 2000), and can approach 10% in the seeds of some plants, where glucosinolates may represent one-half of the sulfur content of the seeds (Josefsson, 1970). Most species contain a limited number of glucosinolates (generally less than one dozen) although as many as 23 different glucosinolates have
Biotic interactions of glucosinolates and isothiocyanates
The antibacterial activities of glucosinolates/isothiocyanates (Kjær and Conti, 1954; Procházka and Komersová, 1959; Virtanen, 1962; Wagner et al., 1965; Dornberger et al., 1975; Johns et al., 1982; Uda et al, 1993; Brabban and Edwards, 1995; Delaquis and Mazza, 1995; Hashem and Saleh, 1999; Lin et al., 2000) and their antifungal activity (Drobinca et al., 1967; Kojima and Ogawa, 1971; Mari et al, 1993; Delaquis and Mazza, 1995; Mayton et al., 1996; Manici et al., 1997; Hashem and Saleh, 1999)
Analytical methods
Since the work of Ettlinger and Lundeen, 1956a, Ettlinger and Lundeen, 1956b, Ettlinger and Lundeen, 1957), much effort has been devoted to developing methods for the efficient isolation and identification of glucosinolates (Betz and Fox, 1994). Most early identifications relied on paper or thin-layer chromatography of the glucosinolates or of their presumptive hydrolysis products (e.g. an investigation of the glucosinolates from the seeds of 151 different crucifers by Danielak and Borkowski,
Glucosinolates/isothiocyanates and cancer chemoprotection
Over the past 20 years, compelling evidence has been obtained linking increased consumption of fruits and vegetables, especially cruciferous vegetables, to reduced incidence of many types of cancer (Steinmetz and Potter, 1991, Steinmetz and Potter, 1996; Block et al., 1992; Doll, 1992; Verhoeven et al., 1996; Michaud et al., 1999; Talalay, 1999). Ingestion of about two servings per day of cruciferous vegetables may result in as much as a 50% reduction in the relative risk for cancer at certain
Concluding remarks
The genus Brassica, represents only 1 of over 350 genera in the Brassicaceae family which, in turn, is only 1 of 16 families of glucosinolate-containing higher plants (Table 3). Many glucosinolate-containing genera contain plants that have been used for food or medicinal purposes by various cultures for many centuries (e.g. capers, Capparis spinosa; wasabi, Wasabia japonica; Arugula, Eruca sativa; Radish, Raphanus sativus) and are currently being investigated for their fungicidal,
Acknowledgements
The assistance of Pamela Talalay, Kristina L. Wade and Katherine K. Stephenson in critical reading of the manuscript and in final manuscript preparation is gratefully acknowledged. Work in the authors’ laboratories was supported by generous gifts from the Lewis and Dorothy Cullman Foundation, Charles B. Benenson and other Friends of the Brassica Chemoprotection Laboratory and by a Program Project grant (PO1 CA 44530) from the National Cancer Institute, Department of Health and Human Services,
References (343)
- et al.
Inhibition of human leukaemia 60 cell growth by mercapturic acid metabolites of phenylethyl isothiocyanate
Food and Chemical Toxicology
(1996) - et al.
Glucosinolates of Egyptian Capparis species
Phytochemistry
(1972) - et al.
The first synthesis of C-glucotropaeolin
Tetrahedron Letters
(1999) - et al.
Protective effects of cruciferous seed meals and hulls against colon cancer in mice
Cancer Letters
(1998) - et al.
Separation by solid phase extraction and quantification by reverse phase HPLC of sulforaphane in broccoli
Food Chemistry
(1998) - et al.
Failure to detect glucosinolates in cocoa
Phytochemistry
(1987) - et al.
Studies on myrosinases: I. Purification and characterization of a myrosinase from white mustard seed (Sinapis alba, L.)
Biochimica et Biophysica Acta
(1972) - et al.
Studies on myrosinases: III. Enzymatic properties of myrosinases from Sinapis alba and Brassica napus seeds
Biochimica et Biophysica Acta
(1973) - et al.
Separation and determination of the intact glucosinolates in rapeseed by high performance liquid chromatography
Journal of Chromatography
(1988) Effects of wounding on glucosinolates in the cotyledons of oilseed rape and mustard
Phytochemistry
(1992)
Potent effect of jasmonates on indole glucosinolates in oilseed rape and mustard
Phytochemistry
Glucosinolates in Bretschneideraceae
Biochemical Systematics and Ecology
Isolation of glucosinolate degrading microorganisms and their potential for reducing the glucosinolate content of rapemeal
FEMS Microbiology Letters
Glucosinolates in 2 Jamaican Capparis species
Phytochemistry
Control of soil-borne plant pests using glucosinolate-containing plants
Advances in Agronomy
The role of indole glucosinolates in the club root disease of the Cruciferae
Physiological Plant Pathology
Exploring an alternative approach to the synthesis of arylalkyl and indolylmethyl glucosinolates
Tetrahedron
Biosynthesis of 3-methylthiopropylglucosinolate and 3-methylsulfinylpropylglucosinolate in wallflower Cheiranthus kewensis
Phytochemistry
Biosynthesis of 3-methoxycarbonylpropyl-glucosinolate in an Erysimum species
Phytochemistry
Mass-spectrometric characteristics of some pertrimethyl-silylated desulfoglucosinolates
Tetrahedron
Isothiocyanates, nitriles, and thiocyanates as products of autolysis of glucosinolates in Cruciferae
Phytochemistry
Treatment of recurrent respiratory papillomatosis with indole-3-carbinol
American Journal of Otolaryngology
Synthesis of 2-deoxy-2-fluoro-glucotropaeolin, a thioglucosidase inhibitor
Carbohydrate Research
Crambe abyssinica meal as starting material for the production of enantiomerically pure fine chemicals
Industrial Crops and Products
Synthesis of glucosinolate precursors and investigations into the biosynthesis of phenylalkyl- and methylthioalkylglucosinolates
Journal of Biological Chemistry
3-Hydroxypropyl glucosinolate, a new glucosinolate in seeds of Erysimum hieracifolium and Malcolmia maritima
Phytochemistry
Glucosinolate composition of seeds from 297 species of wild plants
Phytochemistry
Isothiocyanates, thiourees, et thiocarbamates isoles de Pentadiplandra brazzeana
Phytochemistry
A novel sulphonated natural indole
Phytochemistry
Antioxidant functions of sulforaphane: a potent inducer of Phase 2 detoxication enzymes
Food and Chemical Toxicology
Practical synthesis of sinigrin
Journal of Carbohydrate Chemistry
Naturally occurring glucosinolates with special references to those of family Capparidaceae
Planta Medica
The biosystematics of the genus Thelypodium (Cruciferae)
Contribution, Gray Herbarium Harvard University
CYP2E1-mediated mechanism of anti-genotoxicity of the broccoli constituent sulforaphane
Carcinogenesis
A new mustard oil glucoside synthesis: the synthesis of glucotropaeolin
Canadian Journal of Chemistry
The synthesis of glucoapparin
Canadian Journal of Chemistry
Synthesis of thiohydroximates
Canadian Journal of Chemistry
The synthesis of sinigrin
Journal of the Chemical Society, Chemical Communications
Glucoputranjivin
Canadian Journal of Chemistry
The synthesis of glucocochlearin
Canadian Journal of Chemistry
Aldoxime-forming microsomal enzyme systems involved in the biosynthesis of glucosinolates in oilseed rape (Brassica napus) leaves
Plant Physiology
Glucosinolate biosynthesis: further characterization of the aldoxime-forming microsomal monooxygenases in oilseed rape leaves
Plant Physiology
High performance liquid chromatographic determination of glucosinolates in Brassica vegetables
Antinutritional and toxic effects in rats of individual glucosinolates (± myrosinases) added to a standard diet: 1. Effects on protein utilization and organ weights
Zeitschrift für Tierphysiologie, Tierernährung und Futtermittelkunde
Aromatic hydrocarbon responsiveness-receptor agonists generated from indole-3-carbinol in vitro and in vivo: Comparisons with 2,3,7,8-tetrachlorodibenzo-p-dioxin
Proceedings of the National Academy of Science of the USA
Isolation of intact glucosinolates by column chromatography and determination of their purity
First synthesis of alpha-glucosinolates
Tetrahedron Letters
Fruit, vegetables, and cancer prevention: a review of the epidemiological evidence
Nutrition and Cancer
Isolation and characterization of glucocapparin in Isomeris arborea Nutt
Journal of Chemical Ecology
Cited by (2350)
The chemical composition of the aerial parts’ essential oil of matthiola fruticulosa (L.) maire growing in Sicily, Italy
2024, Natural Product ResearchExploring the mechanism of blindness physiopathy in Brassica oleracea var italica L. by comprehensive transcriptomics and metabolomics analysis
2024, Plant Physiology and BiochemistryEffect of fermentation on chemical and bioactive properties and phenolic profiles of caper (Capparis ovata Desf. var. ovata) flower buds in three different sizes
2024, Journal of the Saudi Society of Agricultural SciencesEngineering Brassica Crops to Optimize Delivery of Bioactive Products Postcooking
2024, ACS Synthetic Biology
- ☆
This paper is dedicated to Professor Anders Kjær, who, with his collaborators in Lyngby, Denmark, has contributed immeasurably to the scientific community’s understanding of glucosinolates and to knowledge of their chemistry, biosynthesis, metabolism, and their relationship to the plants from which they were isolated; more glucosinolates have been isolated and characterized in Professor Kjær’s laboratory than anywhere else in the world.
- 1
Present address: Jefferson Medical College, Thomas Jefferson University, 1020 Locust Street, Philadelphia, PA 19107, USA.