Elsevier

Phytochemistry

Volume 57, Issue 3, June 2001, Pages 325-339
Phytochemistry

Review
Phytoecdysteroids: biological aspects

https://doi.org/10.1016/S0031-9422(01)00078-4Get rights and content

Abstract

Phytoecdysteroids are a family of about 200 plant steroids related in structure to the invertebrate steroid hormone 20-hydroxyecdysone. Typically, they are C27, C28 or C29 compounds possessing a 14α-hydroxy-7-en-6-one chromophore and A/B-cis ring fusion (5β-H). In the present review, the distribution, biosynthesis, biological significance and potential applications of phytoecdysteroids are summarised.

The structural diversity, biosynthesis, possible functions and applications of phytoecdysteroids are reviewed.

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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.

References (172)

  • F Camps et al.

    Ecdysteroid production in tissue cultures of Polypodium vulgare

    Phytochemistry

    (1990)
  • F Camps et al.

    Insect allelochemicals from Ajuga plants

    Phytochemistry

    (1993)
  • C.Y Clément et al.

    Assessment of a microplate-based bioassay for the detection of ecdysteroid-like or antiecdysteroid activities

    Insect Biochemistry and Molecular Biology

    (1993)
  • M.F Corio-Costet et al.

    Sterol and ecdysteroid profiles of Serratula tinctoria (L.): plant and cell cultures producing steroids

    Insect Biochemistry and Molecular Biology

    (1993)
  • C Descoins et al.

    Electrophysiological responses of gustatory sensilla of Mamestra brassicae (Lepidoptera, Noctuidae) larvae to three ecdysteroidsecdysone, 20-hydroxyecdysone and ponasterone A

    Journal of Insect Physiology

    (1999)
  • T.P Devarenne et al.

    Biosynthesis of ecdysteroids in Zea mays

    Phytochemistry

    (1995)
  • L Dinan et al.

    Taxonomic distribution of phytoecdysteroids in seeds of members of the Chenopodiaceae

    Biochemical Systematics and Ecology

    (1998)
  • Y Fujimoto et al.

    Biosynthesis of 20-hydroxyecdysone in Ajuga hairy rootshydrogen migration from C-6 to C-5 during cis-A/B ring formation

    Tetrahedron Letters

    (1997)
  • A Fukuzawa et al.

    Ecdysone-like metabolites, 14α-hydroxypinnasterols, from the red alga Laurencia pinnata

    Phytochemistry

    (1986)
  • R.J Grebenok et al.

    Ecdysteroid distribution during development of spinach

    Phytochemistry

    (1991)
  • R.J Grebenok et al.

    Ecdysteroid biosynthesis during ontogeny of spinach leaves

    Phytochemistry

    (1993)
  • R.J Grebenok et al.

    Ecdysone 20-monooxygenase, a cytochrome P450 enzymes from spinach, Spinacia oleracea

    Phytochemistry

    (1996)
  • R.J Grebenok et al.

    Biosynthesis of ecdysone and ecdysone phosphates in spinach

    Phytochemistry

    (1994)
  • M.L Grieneisen

    Recent advances in our knowledge of ecdysteroid biosynthesis in insects and crustaceans

    Insect Biochemistry and Molecular Biology

    (1994)
  • M.L Grieneisen et al.

    A putative route to ecdysteroidsmetabolism of cholesterol in vitro by mildly disrupted prothoracic glands of Manduca sexta

    Insect Biochemistry

    (1991)
  • R Hyodo et al.

    Biosynthesis of 20-hydroxyecdysone in Ajuga hairy rootsthe possibility of 7-ene introduction at a late stage

    Phytochemistry

    (2000)
  • I Kubo et al.

    Effects of ingested phytoecdysteroids on the growth and development of two lepidopterous larvae

    Journal of Insect Physiology

    (1983)
  • G Kusano et al.

    Steroidal constituents of Solanum xanthocarpum

    Phytochemistry

    (1975)
  • R Lafont et al.

    Standardized abbreviations for common ecdysteroids

    Insect Biochemistry and Molecular Biology

    (1993)
  • R Lafont et al.

    Chromatographic procedures for phytoecdysteroids

    Journal of Chromatgraphy

    (1994)
  • G.H Lüers et al.

    Reporter-linked monitoring of transgene expression in living cells using the ecdysone-inducible promoter system

    European Journal of Cell Biology

    (2000)
  • T.C McMorris et al.

    Ecdysones from gametophytic tissues of a fern

    Phytochemistry

    (1971)
  • Abubakirov, N.K., 1982. Ecdysteroids of flowering plants (Angiospermae). Proceedings of Indian National Science Academy...
  • J.H Adler et al.

    Biosynthesis and distribution of insect-molting hormones in plants — a review

    Lipids

    (1995)
  • V.U Ahmad et al.

    An antimicrobial ecdysone from Asparagus dumosus

    Fitoterapia

    (1996)
  • C Albanese et al.

    Sustained mammary gland-directed, ponasterone A-inducible expression in transgenic mice

    FASEB Journal

    (2000)
  • E.N Anufrieva et al.

    The content and composition of ecdysteroids in plants and tissue cultures of Serratula coronata

    Russian Journal of Plant Physiology

    (1998)
  • C Arnault et al.

    Dietary effects of phytoecdysones in the leek-moth, Acrolepiopsis assectella Zell. (Lepidoptera: Acrolepiidae)

    Journal of Chemical Ecology

    (1986)
  • Badal'yants, K.L., Nabiev, A.N., Khushbaktova, Z.A., Syrov, V.N., 1996. Mechanism of hepatoprotective action of...
  • U.A Baltayev

    Phytoecdysteroids of Rhaponticum carthamoides. III. Rapisterone C

    Khimiya Prirodnykh Soedinenii

    (1992)
  • M Báthori et al.

    Complex phytoecdysteroid cocktail of Silene otites (Caryophyllaceae)

    Archives of Insect Biochemistry and Physiology

    (1999)
  • M Báthori et al.

    Isolation and structural elucidation of two ecdysteroids, gerardiasterone and 22-epi-20-hydroxyecdysone

    Journal of Natural Products

    (1998)
  • R Bergamasco et al.

    The biological activities of ecdysteroids and ecdysteroid analogs

  • Bergamasco, R., Horn, D.H.S., 1983. Distribution and role of insect hormones in plants. In: Endocrinology of Insects,...
  • M.J.P Blackford et al.

    Distribution and metabolism of exogenous ecdysteroids in the Egyptian Cotton Leafworm Spodoptera littoralis (LepidopteraNoctuidae)

    Archives of Insect Biochemistry and Physiology

    (1997)
  • M Blackford et al.

    The effects of ingested ecdysteroid agonists (20-hydroxyecdysone, RH5849 and RH5992) and an ecdysteroid antagonist (cucurbitacin B) on larval development of two polyphagous lepidopterans (Acherontia atropos and Lacanobia oleracea)

    Entomologia Experimentalis et Applicata

    (1997)
  • A Butenandt et al.

    Über die Isolierung eines Metamorphose-hormons der Insekten in kristallisierter Form

    Zeitschrift für Naturforschung

    (1954)
  • F Camps

    Plant ecdysteroids and their interactions with insects

  • L Canonica et al.

    Structure of calonysterone, an unusually modified phytoecdysone

    Journal of the Chemical Society Chemical Communications

    (1973)
  • L Cherbas et al.

    The morphological response of Kc-H cells to ecdysteroidshormonal specificity

    Wilhelm Roux's Archives Developmental Biology

    (1980)
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