ReviewRecent advances in betalain research
This review describes structure elucidation of betalains published within the last decade. Recent advances in betalain biosynthesis are also covered, i.e. enzymatic steps of ‘early’ (dopa formation) and ‘late’ reactions (glucosylation and acylation) as well as non-enzymatic steps (cyclo-dopa and aldimine formation).
Introduction
Betalains are water-soluble nitrogen-containing pigments, which comprise the red-violet betacyanins and the yellow betaxanthins. They are immonium conjugates of betalamic acid with cyclo-dopa and amino acids or amines, respectively. The structure scheme shows betalamic acid (1), the chromophore of all betalains, betanidin (2) (Wyler et al., 1963), the aglycone of most of the betacyanins, and indicaxanthin (3) (Piattelli et al., 1964), a proline-containing betaxanthin. These were the first betalains identified by chemical means. Since then, betaxanthins with various other amino acids and amines as well as various betanidin conjugates (glycosides and acylglycosides) were identified by spectroscopic techniques (Strack et al., 1993, Strack and Wray, 1994a).
Within the last decade, a series of publications has described new structures and complete identification of some putative ones as well as elucidation of biosynthetic reactions (Roberts and Strack, 1999). Some early enzymatic reactions in betalain biosynthesis were characterized, polyphenoloxidase (PPO)-type tyrosinase and extradiolic dopa dioxygenase. Furthermore, the decisive steps in the biosynthesis of both betanidin and betaxanthins by aldimine formation were recently identified to proceed non-enzymatically. Finally, betalain-specific glucosyl- and hydroxycinnamoyltransferases were characterized.
Betalains accumulate in flowers, fruits and occasionally in vegetative tissues of plants belonging to most families of the Caryophyllales (Steglich and Strack, 1990). However, there are two exceptions: the Caryophyllaceae and the Molluginaceae accumulate anthocyanins instead, flavonoid-derived pigments occurring in all other families of flowering plants. The Caryophyllales-specific occurrence of betalains is a prominent example of the chemotaxonomic relevance of plant secondary products. Gain and loss of anthocyanins and betalains during plant evolution still remain a mystery (Clement and Mabry, 1996). Molecular studies are needed to elucidate the evolutionary mechanisms leading to the mutual exclusion of the betalain and anthocyanin pathways in flowering plants (Kimler et al., 1970, Stafford, 1994). Betalains were also detected in some higher fungi (Steglich and Strack, 1990), for example in the fly agaric (Amanita muscaria). Whereas the functions of betalains in plant flower and fruit colouration are obvious, their role in fungi is unknown.
There is growing interest in the use of natural pigments for food colouring, since synthetic dyes are becoming more and more critically assessed by the consumer. In food processing, betalains are less commonly used than anthocyanins and carotenoids, although these water-soluble pigments, stable between pH 3 and 7, are well suited for colouring low acid food. The most important source of betanin (4) as colouring agent is the red beet (Beta vulgaris subsp. vulgaris) root. The corresponding cell cultures (Leathers et al., 1992, Trejo-Tapia et al., 1999, Akita et al., 2000) and hairy roots (Mukundan et al., 1998a, Mukundan et al., 1998b, Berzin et al., 1999) cannot compete with the plant's root (50-60 t/ha with ca. 0.5 g betanin/kg) (Stintzing et al., 2000) with respect to betanin accumulation. Besides betanin from red beet, also betacyanins from plants of the Amaranthaceae were tested concerning colour properties and pigment stability in model food systems (Cai et al., 1998, Cai and Corke, 1999, Cai and Corke, 2000).
Betacyanins are a class of compounds with antioxidant and radical scavenging activities (Pedreni ands Escribano, 2000, Escribano et al., 1998, Kanner et al., 2001). It is known that they prevent oxidative processes, which contribute to the onset of several degenerative diseases in human. Since betanin exerts a good bioavailability, red beet products may provide protection against certain oxidative stress-related disorders (Kanner et al., 2001).
Section snippets
Isolation and structure elucidation
The methods recommended for analytical characterization, preparative isolation, photometric quantification and structure elucidation of betalains, the latter mainly by MS- and NMR-techniques, are comprehensively summarized in two reviews (Strack et al., 1993, Strack and Wray, 1994a).
Extraction of betalains from plant tissues or cell cultures is commonly performed with aqueous methanol; however, the addition of ascorbic acid (ca. 50 mM) in the extraction medium is recommended (Schliemann et al.,
Biochemistry
The biosynthetic steps involved in betalain biosynthesis are summarized in Fig. 8. While some ‘early’ and ‘late’ reactions are enzymatically catalysed, the intermediate steps (cyclizations, X–XIII; aldimine formation, XIV–XVIII) are assumed to proceed spontaneously, i.e. formation of cyclo-dopa via dopaquinone, betalamic acid via 4,5-seco-dopa, muscaflavin via 2,3-seco-dopa and the condensations of betalamic acid with cyclo-dopa (betanidin formation) or amino acids/amines (betaxanthin
Acknowledgements
The investigations at Halle have been supported by the Deutsche Forschungsgemeinschaft (Bonn). We are grateful to Christine Kaufmann for the graphics and to Annett Kohlberg for the photographs.
Dieter Strack graduated in 1973 in botany at the University of Cologne and spent one year as a postdoctoral fellow at the University of South Florida in Tampa. He then returned to his university and became Assistant Professor. After holding a Heisenberg scholarship from the Deutsche Forschungsgemeinschaft (Bonn) he received in 1987 a professorship at the Institute of Pharmaceutical Biology of the Technical University Braunschweig. In 1993 he was appointed Head of the Department of Secondary
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Dieter Strack graduated in 1973 in botany at the University of Cologne and spent one year as a postdoctoral fellow at the University of South Florida in Tampa. He then returned to his university and became Assistant Professor. After holding a Heisenberg scholarship from the Deutsche Forschungsgemeinschaft (Bonn) he received in 1987 a professorship at the Institute of Pharmaceutical Biology of the Technical University Braunschweig. In 1993 he was appointed Head of the Department of Secondary Metabolism at the Leibniz Institute of Plant Biochemistry (IPB) in Halle (Saale). He also holds a professorship at the Institute of Pharmaceutical Biology of the University Halle-Wittenberg and was recently appointed Honorary Professor at the University of Leipzig. His work is concerned with structure elucidation, enzymology and molecular biology of plant secondary products, focusing on hydroxycinnamic acids, betalains and (apo)carotenoids. The latter is part of his interest in mutualistic associations between plant roots and mycorrhizal fungi (arbuscular mycorrhizas). His interest in betalains was stimulated by Professor Hans Reznik, who was supervisor of his doctoral thesis in Cologne.
Thomas Vogt completed his doctoral degree in botany at the University of Cologne in 1989, working on flavonoids in Mediterranean plants. Sponsored by the Alexander-von-Humboldt Foundation, he spent two years as a post-doc at the University of British Columbia in Vancouver, Canada, with Brian Ellis working on sinapine biosynthesis in rapeseed. He moved to Washington State University, Pullman, U.S.A., to work on flavonoid-stimulated pollen germination in Petunia with Loverine Taylor, before he joined the Department of Secondary Metabolism at the IPB in Halle (Saale) in 1993. His research group focuses on biochemical, molecular and phylogenetic aspects of natural product modification, with specific emphasis on glucosyltransferases involved in betalain biosynthesis.
Willibald Schliemann graduated in 1972 in pharmaceutical chemistry at the University Halle-Wittenberg. After being employed two years each at the Institute of Clinical Biochemistry, in the chemical industry and at a Blood Transfusion Center, he started to work at the Institute of Biochemistry of Plants in Halle (Saale) in 1977. His first research interest focused on phytohormones, especially gibberellin conjugates. After the reunification of Germany he joined the Department of Secondary Metabolism at the IPB to work with Professor Dieter Strack on structure elucidation and biosynthesis of betalains. Recently he became group leader working on metabolomics in research on the biochemistry of arbuscular mycorrhizas.