ReviewPhytoecdysteroids: biological aspects
The structural diversity, biosynthesis, possible functions and applications of phytoecdysteroids are reviewed.
Introduction
Ecdysteroids were first recognised as steroidal hormones controlling moulting and metamorphosis in insects. Today, it is realised that these steroids are present at all stages of insect development, regulating many biochemical and physiological processes: in newly-laid eggs, during embryonic and postembryonic developments and in adult insects, regulating aspects of development, metamorphosis, reproduction and diapause. Ecdysteroids are the steroid hormones of all classes of arthropods and probably of other invertebrates too (see Koolman, 1989, for reviews). Analogues of ecdysteroids (phytoecdysteroids) also occur in a certain proportion of plant species. Their function in plants is still conjectural, but it is believed that they provide some degree of protection against non-adapted phytophagous insects and/or soil nematodes (Bergamasco and Horn, 1983, Kubo and Hanke, 1986). The first ecdysteroid, ecdysone (E), was isolated by Butenandt and Karlson (1954) from silkworm pupae and its structure was finally elucidated in 1965 by means of X-ray crystallography (Huber and Hoppe, 1965). Subsequently, 20-hydroxyecdysone (Fig. 1; 20E; see Lafont et al., 1993, for standardised abbreviations for ecdysteroids) was identified from a number of arthropod sources and this compound is now generally recognised as the major biologically active ecdysteroid in most invertebrate systems, although this does not exclude the possibility that other ecdysteroids may be active in certain types of invertebrate or at specific stages of development. The first isolations of ecdysteroids from plant sources were a rather remarkable coincidence. While investigating the chemical constituents of the leaves of Podocarpus nakaii for antitumour agents, Nakanishi et al. (1966) isolated three polyhydroxylated steroids (ponasterones A, B and C). At almost the same time, Takemoto's group isolated 20E and inokosterone from the roots of Achyranthes fauriei (Takemoto et al., 1967). Likewise, 20E was found in the wood of Podocarpus elatus (Galbraith and Horn, 1966), the rhizomes of Polypodium vulgare (Heinrich and Hoffmeister, 1967) and in dry pinnae of Pteridinium aquilinum (Kaplanis et al., 1967). These early reports stimulated further research and it soon became apparent that ecdysteroids were rather widespread in plants (reviewed in Hikino and Hikino, 1970, Horn, 1971, Nakanishi, 1971, Nakanishi, 1992, Prakash and Ghosal, 1979, Hetru and Horn, 1980, Abubakirov, 1982, Ohsawa et al., 1992, Horn and Bergamasco, 1985, Kubo and Hanke, 1986, Lafont, and Horn, 1989, Camps, 1991, Lafont and Wilson, 1996). Since the discovery of ecdysteroid analogues in plants, it has been convenient to designate these as phytoecdysteroids to differentiate them from those isolated from insects, crustaceans and other animal sources (zooecdysteroids). However, this division must be regarded as non-exclusive, since many ecdysteroids (e.g. E, 20E, makisterone A, ajugasterone C) are present in both animals and plants. This review will consider the distribution of ecdysteroids in the plant world, their structural diversity, biosynthesis, possible functions and also their potential agrochemical and medicinal applications. Emphasis will be placed on the more recent literature. The reader is referred to the excellent reviews listed above for earlier literature.
Section snippets
Distribution of ecdysteroids in the plant world
Phytoecdysteroids (PEs) have been reported to occur in over 100 terrestrial plant families representing ferns, gymnosperms and angiosperms. They are found in both annuals and perennials. The ecdysteroid-like compound 14α-hydroxypinnasterol (like 20E, but having unsaturation at C-4 and a 3α-hydroxyl function, yet lacking a 25-hydroxyl group) and related compounds have been also characterized from the red marine alga Laurencia pinnata (Fukuzawa et al., 1986). In both an early survey of Japanese
Structural diversity
A compilation of known ecdysteroid structures up to 1995 has been published (Lafont and Wilson, 1996). Structural diversity among (phyto)ecdysteroids has been previously reviewed (Hetru and Horn, 1980, Lafont, and Horn, 1989, Lafont, et al., 1991, Lafont, 1997, Lafont, 1998). In the following discussion, references are cited for PEs which appeared in the literature after 1995; for compounds first published prior to this, the reader is referred to The Ecdysone Handbook (Lafont and Wilson, 1996).
Phytoecdysteroid production in vitro
The occurrence of ecdysteroids in callus cultures was first described for seedling callus tissues from several Achyranthes species (Hikino et al., 1971) and Trianthema portulacastrum (Ravishankar and Metha, 1979). PEs have also been isolated from the culture filtrates of Ajuga turkestanica (Lev et al., 1990), A. reptans var. atropurpurea (Matsumoto and Tanaka, 1991), Pteridium aquilinum (McMorris and Voeller, 1971) and Serratula tinctoria (Corio-Costet et al., 1996). 20E was produced at a two-
Biosynthesis
Our understanding of the biosynthetic pathway(s) for ecdysteroids in plants is limited. In part, this was a consequence of the lack of convenient study systems, a situation which is beginning to change with the application of amenable in vitro systems, such as hairy root cultures or cell suspension cultures. In view of the potential applications of PEs in crop protection (see below) it is surprising that more emphasis has not been placed on the elucidation of the biosynthetic pathway(s) for
Biological significance of phytoecdysteroids to plants
The importance of the ecdysteroids in the life-cycle of plants has not been fully elucidated. There are two main hypotheses. The first is that PEs have a hormonal role within the plant, but there is very little hard evidence in support of this hypothesis and quite a lot against it (reviewed in Dinan, 1998). Alternatively, it has long been recognised that PEs possess insect moulting hormone activity and they could participate in the defence of plants against non-adapted phytophagous
Structure–activity studies
It is often presumed that most, if not all, ecdysteroid responses are mediated by intracellular ecdysteroid receptor complexes, of which the two main components (the EcR and USP proteins) belong to the nuclear receptor superfamily (Yao et al., 1993), and which modify the activity of specific gene sets. However, it should be mentioned that evidence is accumulating that ecdysteroids may also have non-genomic effects (reviewed in Tomaschko, 1999). Consequently, SAR studies can be strongly
Applications of phytoecdysteroids
Since the discovery of large amounts of ecdysteroids in plants (relative to the much lower concentrations found in most animal sources), PEs have been purified for use in biochemical and physiological experiments in invertebrate systems. In fact, it is fair to say that our knowledge of the role of ecdysteroids in insect endocrinology would be much poorer if it had not been for the availability of ecdysteroids (especially 20E, E and ponA) from plant sources. In recent years, however, new areas
Concluding remarks
PEs are attracting renewed attention because of their specific effects on invertebrate development (potential in invertebrate pest control) and their varied benign pharmacological actions on mammals (biomedical applications and gene switches). In the past three decades, several thousand species of plants have been surveyed for the presence of PEs and the structures of over 200 PEs have been deduced. The most frequently encountered PE is 20E, the principal physiological inducer of moulting and
Acknowledgements
Research in Exeter was supported by the Biotechnology and Biological Sciences Research Council of the UK, EU-INTAS (Contract 96-1291) and Rohm & Haas Co. (Spring House, PA, USA). I thank Pauline Bourne for reading and commenting on the manuscript.
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