Plant ecdysteroids: plant sterols with intriguing distributions, biological effects and relations to plant hormones
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The present review summarises current knowledge of phytoecdysteroids’ biosynthesis, distribution within plants, biological importance and relations to plant hormones.
Plant ecdysteroids (phytoecdysteroids) are natural polyhydroxylated compounds that have a four-ringed skeleton, usually composed of either 27 carbon atoms or 28–29 carbon atoms (biosynthetically derived from cholesterol or other plant sterols, respectively). Their physiological roles in plants have not yet been confirmed and their occurrence is not universal. Nevertheless, they are present at high concentrations in various plant species, including commonly consumed vegetables, and have a broad spectrum of pharmacological and medicinal properties in mammals, including hepatoprotective and hypoglycaemic effects, and anabolic effects on skeletal muscle, without androgenic side-effects. Furthermore, phytoecdysteroids can enhance stress resistance by promoting vitality and enhancing physical performance; thus, they are considered adaptogens. This review summarises current knowledge of phytoecdysteroids’ biosynthesis, distribution within plants, biological importance and relations to plant hormones.
KeywordsPhytoecdysteroids Ecdysteroids 20-Hydroxyecdysone Plant hormones Signalling molecules
2,4-Dichlorophenoxy acetic acid
Distribution of phytoecdysteroids within plants
Phytoecdysteroids are frequently detectable in newly emerged tissues (young leaves) and reproductive organs (flowers, anthers, seeds) of annual plants, but less frequently in stems and roots (Dinan et al. 2001). This may imply that the highest concentrations of PEs are found in tissues that are important for plants’ survival or organs needed for the next generation of plants (Dinan et al. 2009). This is in accordance with the hypothesis that PEs may serve as protectors against predators (discussed in more detail below in the section “Biological importance of phytoecdysteroids”). Results consistent with this hypothesis have been obtained for Chenopodium album, where levels of PEs are reportedly highest in the anthers (protecting developing pollen), seeds and young leaves (Dinan 1992). In addition, cotyledons and the first two true leaves of spinach (another annual plant with rich PEs content) can reportedly synthesise PEs more rapidly and abundantly than later leaves (Grebenok and Adler 1993).
Comparing distribution of PEs in annual and perennial plants, it is believed that annual plants transfer PEs present in seeds to the developing shoots at the beginning of their growth (Grebenok et al. 1991), while many perennials (e.g. the Siberian herb Maral root Leuzea carthamoides) cycle PEs between their underground (perennial) and aerial part (deciduous) during the season, i.e. in spring the highest concentration of PEs can be found in the newly developing shoot while in autumn, the PEs are transferred from the shoot to the root where their level rises (Kholodova et al. 1979).
Biosynthesis of phytoecdysteroids
In spite of many biosynthetic studies aiming to reveal biochemical background of ECs formation and published during last three decades, our understanding of the biosynthetic pathway(s) for these compounds still remains limited. This is especially true for PEs biosynthesis since these studies have been focused more to the ECs biosynthesis in invertebrates while only small attention has been paid to PEs synthesis in plants. To our knowledge, the sites of PEs production have not been found yet and it is not even known if their biosynthesis takes place only in specialised cells or in all cells of particular tissue/organism. Only biosynthetic enzyme purified so far is ecdysone 20-monooxygenase catalysing the oxidation of E to 20E (Fig. 2; Grebenok et al. 1996; Canals et al. 2005). This compound is Δ7 sterol possessing a reduced side chain at C-24 (Fig. 1). From this point of view, its precursor for its biosynthesis should be also C-24 reduced Δ7 sterol. This hypothesis has been confirmed using spinach as a model plant where lathosterol has been found as Δ7 sterol reduced at C-24 as already mentioned above (Grebenok and Adler 1993). Δ7 sterols are also found in related chenopods (Salt and Adler 1985) and in some other plant families (Nes 1977). Nevertheless, many other plants have been reported to possess C-24 alkylated PEs (Horn and Bergamasco 1985) being presumably formed from C-24 alkylated sterols. These plants produce 24-alkyl Δ5 sterols as well as cholesterol that is not alkylated at C-24 (Fig. 2). It is not, however, known whether cholesterol or lathosterol is the preferred substrate for PEs biosynthesis. Both these sterols have been reported to be present for instance in Chenopodium album and Chenopodium quinoa (Xu et al. 1990).
Biological importance of phytoecdysteroids
Unlike the very well-known hormonal activity of ECs in animals, there are numerous indications that plant ecdysteroids do not possess hormonal activity in planta. Notably, they have at most slight activity in various plant hormone activity assays (for instance, auxin, cytokinin, brassinosteroid and gibberellin bioassays) (Hendrix and Jones 1972; Dreier and Towers 1988; Macháčková et al. 1995). These results are consistent with apparently not universal PEs’ presence in terrestrial plant species tested to date. However, this only accounts for less than 2 % of the global flora (Dinan 2001) and, as mentioned above, methods routinely used for their detection may be insufficiently sensitive. Furthermore, PE levels in PE-positive plants are often much higher than the trace levels of phytohormones, e.g., 1–2 % dry weight in Leuzea carthamoides (Koudela et al. 1995), and no PE receptor has been reported to date. The only known ecdysteroid-binding proteins are members of the nuclear receptor superfamily with a characteristic domain structure in arthropods (Laudet 1997). For all these reasons, PEs are usually regarded as plant secondary metabolites, and not plant hormones. Despite their non-hormonal properties in plants, PEs seem to participate in the regulation of some physiological processes in photosynthesizing organisms. For example, they appear to influence the size and growth of cells of the alga Chlorella vulgaris (Bajguz and Dinan 2004) and growth of the cyanobacterium Nostoc (Maršálek et al. 1992). The main hypothesis regarding the function of PEs in plants is that they provide protection against non-adapted insects (invertebrates) and/or soil nematodes (Bergamasco and Horn 1983; Kubo and Hanke 1986). Thus, increasing plants’ endogenous PEs levels, or modulating their PEs profiles, by breeding or genetic modification, could provide potent strategies for protecting some crop plants. PEs acting either alone or in concert with other signalling molecules may deter consumption of plants (antifeedants), or lead to endocrine disruption and/or death of phytophagous invertebrates. This hypothesis is supported by results of several experiments involving either PEs exogenous applications or transgenic/mutant plants with elevated endogenous PEs levels. For instance, Udalova et al. (2004) found that spraying tomato plants with a solution of αα-ecdysone reduced infestation by the root-knot nematode Meloidogyne incognita. Similarly, Soriano et al. (2004) found that exposing cereal cyst nematodes to exogenously applied 20E at concentrations higher than 10−6 M greatly reduced their capacity to invade wheat roots. Furthermore, Schmelz et al. (1999) observed that spinach plants inoculated with two types of cereal cyst nematodes and one type of root-knot nematode were less damaged when levels of endogenous PEs in the plants were elevated by treatment with methyl jasmonate (MeJA). Generally speaking, the production of endocrine disruptors is a common defence mechanism of many plants against plant-eating insects (Bergamasco and Horn 1983). The principle of PEs action as disruptors consists in affecting the growth, development or reproduction of insects. Apparently, PEs do not show any toxicity to mammals (Dinan 2001). The susceptibility of insects to dietary PEs varies depending upon the insect species and the structure of PE (Kubo and Klocke 1983; Horn and Bergamasco 1985; Harborne 1988). For instance, 20E can cause 50 % feeding inhibition for spring wheat aphid (Schizaphis graminum; it can cause yellowing and premature death of wheat leaves) at 650 ppm in the diet, but has no effect on feeding of corn earworm (Heliothis zea; it is polyphagous major agricultural pest resistant to many pesticides and causing corn and other crop plants damage) even at higher concentration (3000 ppm) in the diet (Kubo and Klocke 1983). Further, the experiments with pink bollworm Pectinophora gossypiella revealed that 20E is capable to inhibit 95 % ecdysis of this organism at 50 ppm while 20E analogue called ponasterone A (ponA; missing hydroxyl group at position C-25—Fig. 1) is already effective at concentration of 2 ppm (Kubo and Klocke 1983).
Some PEs produced by plants also appear to act as allelochemicals, i.e., chemicals that are released by plants into the soil and stimulate or impair the growth and/or development of neighbouring organisms (plants, insects, fungi or other microbes). For example, PEs including 20E and its acetonides isolated from leaves of Chenopodium album reportedly influence seed germination and seedling growth of both monocotyledonous (onion) and dicotyledonous (lettuce and tomato) plants (DellaGreca et al. 2005; Bakrim et al. 2007). Furthermore, experiments with PE extracts containing 20E from the monocotyledon Asparagus dumosus (used in traditional Asian medicine, mainly as a diuretic and antiseptic agent) indicate that 20E appears to have antibacterial and antifungal properties (Ahmad et al. 1996). In addition, seeds of quinoa (Chenopodium quinoa Willd., Amaranthaceae), a functional food and nutraceutical, have very high contents of PEs (mainly 20E), 4–12 times more than spinach (Kumpun et al. 2011), and compounds secreted by intact quinoa seeds into water during initial stages of germination reportedly have anti-diabetic properties, as they can significantly lower fasting blood glucose in obese, hyperglycemic mice (Graf et al. 2014). Other therapeutic properties in mammals—including anabolic, performance-enhancing, anti-osteoporotic and wound healing effects—have also been described by various authors (e.g., Slama and Lafont 1995; Kapur et al. 2010; Seidlova-Wuttke et al. 2010; Syrov and Khushbaktova 1996; Lafont and Dinan 2003).
Last, but not least, there are indications that PEs participate in regulation of photosynthesis in plants. Holá et al. (2013) found that exogenous application of 20E to leaves of Tetragonia tetragonioides (New Zealand spinach) enhances their net photosynthetic rate (P N), but not their photosynthetic electron transport rate or content of photosynthetic pigments. The increase in P N was statistically significant during the 4–6 h after treatment, but not later. Moreover, the first phase of the Calvin cycle (light-independent reactions of photosynthesis)—fixation of CO2 into organic matter—is also positively affected by exogenous application of some PEs (Macek et al. 2008; Holá et al. 2012). During the first Calvin cycle reaction, the enzyme RuBisCO (ribulose-1,5-bisphosphate carboxylase/oxygenase) catalyses carboxylation of ribulose-1,5-bisphosphate, RuBP, by CO2, and exogenously applied 20E can increase the RuBP yield (most strongly with equimolar concentrations of 20E and RuBisCO under in vitro conditions).
Relations of phytoecdysteroids and plant hormones
Nine groups of plant hormones have been identified and studied to date: auxins, cytokinins, gibberellins, abscisic acid, jasmonates, ethylene, brassinosteroids and (the most recently found) strigolactones—signalling molecules expanding the family of isoprenoid plant hormones (Tarkowská et al. 2014). Plants’ intricate signalling networks are further complicated by links and interactions with synthesis and metabolic pathways of secondary metabolites. To date, no review concerning the relations of phytoecdysteroids and plant hormones has been published, but there are some indications that these substances might interact to some extent and thus influence some physiological processes and developmental events in plants. Thus, some information regarding these interactions is summarised here.
Jasmonates—jasmonic acid (JA) and its derivatives—are well-known chemical messengers that play major roles in plant responses to both biotic and abiotic stresses (Wasternack and Hause 2013). JA usually accumulates rapidly in wounded plants following mechanical damage (Glauser et al. 2008; Glauser et al. 2009) or after attacks of plant by herbivorous or phytophagous insects (Howe and Jander 2008). In addition, the volatile methyl ester of JA (MeJA) is usually generated in target plant tissue and plays a key role in rapid transmission of JA signalling (Farmer and Ryan 1990). JA-mediated processes, such as synthesis of defence proteins and biosynthesis of secondary compounds, can be induced by application of exogenous MeJA, which is converted within plants to the biologically active JA-Ile (JA conjugated with the amino acid isoleucine). These responses have been exploited to assess roles and effects of PE induction in plants’ insect protection systems (see above), initially when Schmelz et al. (1998) investigated the phytochemicals that were rapidly induced by damage treatment and applications of MeJA, using hydroponically grown spinach as a model plant. Addition of MeJA to the plants’ root systems stimulated accumulation of root PEs (20E) in a dose-dependent manner, while mechanically damaged roots exhibited two to three fold higher 20E concentrations within 2 days. Forty-eight hours later, small increases of 20E levels in shoots were also detectable, but its concentrations remained unchanged in shoots following shoot herbivory by an insect (Spodoptera exigua). Thus, the cited authors concluded that signals mediating wound-induced accumulation of PEs are transmitted via endogenous JA generated in the roots. Based on these findings and using the same inducible system (induction of 20E production by spinach plants following root damage or MeJA application), the same research group showed that attacks by the dark-winged fungus gnat (Bradysia impatiens) raise 20E levels in spinach roots four- to nearly sevenfold (Schmelz et al. 2002). Moreover, induction of 20E production in roots with MeJA resulted in a twofold increase in 20E levels and 50 % reduction in B. impatiens larval establishment. The cited authors therefore concluded that PEs can act as inducible defences against insect herbivory. This finding was subsequently validated by findings that plant-parasitic nematodes exposed to either exogenous 20E or elevated endogenous levels in plants show abnormal moulting, immobility, reduced invasiveness and impaired development leading to their death (Soriano et al. 2004).
Phytoecdysteroids share some structural resemblance with brassinosteroids (BRs), which show some biological activity in insects as weak ecdysteroid antagonists (Dinan and Hormann 2005). Chemically, both of these triterpenoid families comprise C27 to C29 polyhydroxylated steroids with an oxygenated B-ring. However, the B-ring in BRs often bears a carbonyl group at C-6 and may be expanded to form a lactone (in brassinolide and its analogues), while the ECs have a characteristic 14α-hydroxy-7-en-6-one grouping. Further, hydroxyl groups at C-2, C-3 and C-22 are found in both families, but their orientations and locations of further hydroxyls differ between them. In addition, the junction of the A- and B-rings is in cis-orientation in the skeleton of ECs while BRs have an A/B-trans-configuration. Due to these structural differences BR receptors are unlikely to recognise ECs and vice versa, so plant BR and insect EC receptors show high specificity, explaining why PEs do not interfere with BR signalling pathways in plants where these two families of compounds co-exist. It has been proved that ECs show very weak or no activity in BR-responsive plant bioassays (Dreier and Towers 1988; Macháčková et al. 1995). Similarly, BRs do not interfere with EC signalling in insects (which could otherwise have major effects, as BRs are present, albeit at very low concentrations, in plant tissues consumed by insect herbivores). However, some synthetic structural analogues of both ECs and BRs (castasterone with various modifications) have been prepared to test their potential agonist or antagonist activity (Voigt et al. 2001) in the Drosophila melanogaster BII cell bioassay (for EC activity) and rice lamina inclination bioassay (for BR activity). Only one tested compound showed distinct PE agonist activity, at relatively high concentration (1 × 10−5 M), almost 2000-fold weaker activity than 20E. In the BR bioassay, most of the tested substances showed activity, with indications that biological activity declines with increasing structural deviation of the test compound from castasterone (used as a natural BR standard).
As mentioned above in the “Biological importance of phytoecdysteroids” section, some PEs (notably 20E) can affect various processes associated with photosynthesis, and BRs (at least 24-epibrassinolide, epiBL) share this property. For example, in pea plants, exogenous epiBL induces alterations in the thermodynamic parameters of photosynthetic membranes, reorganisation of the main pigment–protein complexes and partial unstacking of thylakoid membranes (Dobrikova et al. 2014). The cited authors claim that BR-induced changes in photosynthetic membranes are probably involved in the stress tolerance of plants. epiBL can also increase photosynthesis yields at even lower concentrations than the PE concentrations required to affect RuBisCO activity (Rothová et al. 2014). Moreover, exogenously applied epiBL induces changes in PEs contents in plant tissues (Kamlar et al. 2015), to degrees that depend on the developmental stage of leaves (of the same plant) and the epiBL concentration applied (10−8 or 10−6 M in the cited experiments). In control plants, young leaves had ca. sevenfold higher contents of the major PEs than the older leaves. Treatment with epiBL led to a reduction in endogenous 20E content in the young leaves at 10−6 M concentration, but an increase at 10−8 M. These effects were weaker, only temporary and apparent within 4 h of treatment in older leaves. Exogenous epiBL also changed the leaves’ PE profiles. Young leaves of control plants had ca. tenfold higher polypodine B (polB, Fig. 1) contents but twofold lower ajugasterone C (ajuC; Fig. 1) and stachysterone C (stachC; Fig. 1) levels than older leaves (and similar levels of the trace compound ponA). Application of epiBL at 10−6 M led to reductions in stachC and ponA levels, but increases in ajuC abundance (which were stronger when epiBL was applied at 10−8 M). These observations confirm that exogenous BRs can induce detectable changes in levels of individual endogenous PEs in the same tissue within hours.
Cytokinins (CKs) comprise one of the most important classes of endogenous growth- and development-regulating substances in plants. Chemically, they are adenine species substituted at the N6-position with either an isoprenoid or aromatic side-chain. They occur in plant tissues as free species, ribosides, ribotides or glycosides, and have no structural similarity with PEs. Although they are mainly known to have pronounced effects on plant development, at least one CK (isopentenyladenosine, iPR), is also present in animal cells (Faust and Dice 1991). Furthermore, iPR has anti-proliferative activity against mammalian cancer cell lines (Rajabi et al. 2010; Casati et al. 2011). This is not entirely surprising since callus consists of clusters of dedifferentiated plant cells that proliferate indefinitely in a disorganised manner, like human cancer cells, and a signature effect of iPR (and other CKs) is induction of re-differentiation of callus to form adventitious buds (Tanimoto and Harada 1982). Moreover, in insects (traditionally rich sources of ECs) an iPR monophosphate conjugate with ecdysone has been detected. Tsoupras et al. (1983) identified this compound as 22-N 6-(isopentenyl)adenosine monophosphoric ester of ecdysone by mass spectrometry and NMR, and showed that it was present at very high levels (50 nmol/g) in newly laid eggs of the migratory locust (Locusta migratoria). They also found that the eggs contained even higher (more than double) levels of a 2-deoxyecdysone conjugate with adenosine monophosphate (Tsoupras et al. 1982a). Later investigation revealed that this insect can produce adenosine 22-phosphate conjugates of 2-deoxy-20-hydroxyecdysone, 20-hydroxyecdysone and 20-hydroxyecdysone acetate (Tsoupras et al. 1982b). All these conjugates produced by female locusts are further progressively hydrolysed during embryonic development, yielding free highly biologically active hormones (Lagueux et al. 1979). Therefore, it is believed that females of migratory locust and other related insect species (Isaac et al. 1982) serve as suppliers of hormonal molecules for their offspring, which the embryos cannot synthesise de novo before they reach advanced developmental stages. Another indication that CKs may influence the development of insects is that the aromatic CK 6-benzylaminopurine (BAP) can stimulate growth of Drosophila cells (Becker and Roussaux 1981). In addition, dietary provision of another aromatic CK, kinetin (6-furfurylaminopurine, known to delay senescence in plants), can retard ageing of Zaprionus paravittiger fruit flies and prolong their lifespan (Sharma et al. 1995). This anti-ageing effect was attributed to a reduction in age-specific death rates throughout the adult lifespan rather than slowing of development. This study also describes retardation of the larval and pupal stages of the developing insects by kinetin. Overall, the findings summarised in this section indicate that interactions between CKs and ECs warrant further attention.
Three major PEs (20E-3-acetate, 20E and its hydroxylated analogue polypodine B) have been found in tissues of the perennial plant Serratula tinctoria and in vitro cultures (cell suspension cultures and calluses) of this plant (Corio-Costet et al. 1993). Supplementation of cultures of this species transformed by Agrobacterium rhizogenes (with a characteristic hairy root phenotype) with the synthetic auxin 2,4-dichlorophenoxy acetic acid (2,4-D) had dose-dependent negative effects on their PE contents. Growth of the hairy roots slowed on media containing 0.05–0.5 mg/l of 2,4-D, and addition of 1 mg/l stopped their growth entirely due to tissue necrosis (Corio-Costet et al. 1996). Reductions in EC concentrations in hairy roots of another plant species (the European herbaceous plant Ajuga reptans) have also been observed following addition of 0.1 mg/l of natural auxin (indole-3-acetic acid, IAA) to the cultivation medium, despite increases in the roots’ growth rate due to increases in the number of root apical meristems (Uozumi et al. 1995). To our knowledge, no published study has addressed effects of exogenously applied ECs on levels of endogenous auxins in planta. Tests of PEs’ auxin-like activity in a wheat coleoptile assay revealed that ecdysone has no biological activity, except slight inhibitory effects at non-physiologically high concentrations (Macháčková et al. 1995). Thus, no notable synergistic or antagonistic relationship between PEs and auxin has been found to date.
Phytoecdysteroids and other plant hormones
We are aware of just one study concerning relations between gibberellins (GAs) and PEs. In this study, Macháčková et al. (1995) found that two insect moulting hormones (20E and E) had no effects in a dwarf maize GA bioassay, but slight gibberellin-like activity in dwarf rice bioassays (0.4- to 4-fold weaker effects than gibberellic acid). Nevertheless, its action was unequivocally and dose-dependently stimulatory in the latter assay, and the results also indicate a slight synergistic action of ecdysone and gibberellic acid.
Infinitesimal stimulation of ethylene production in Chenopodium rubrum and dwarf maize by ecdysone has also been observed in bioassays within 3–5 h of its application. However, this effect subsequently disappeared leading to the conclusion that ecdysone has negligible effects on ethylene production in the test system used. To our knowledge, nothing is known about possible relations between PEs and other plant hormones like abscisic acid and strigolactones.
PEs clearly have intriguing distributions, but their roles in plants are still obscure despite many recent findings. Their likeliest functions still seem to be in defences against insect herbivores, which have potentially profound implications for (and applications in) agriculture. Furthermore, they clearly have potent pharmacological and medicinal properties that warrant much more attention (particularly as plants comprise a major part of human diets). For example, the numerous indications that they are very effective, non-androgenic, adaptogens and elicitors of anabolic effects on skeletal muscle suggest possible uses as natural drugs to boost people’s stress resistance, post-damage muscle regeneration and sports performance. In addition, PE contents of many more plants should be screened, using sensitive modern analytical instruments to allow detection of PEs present at low concentrations to broaden knowledge of their distributions, profiles and roles in both perennial and annual plants. Last, but not least, further analysis of the origin(s) of isoprenoid units used in PEs’ biosynthesis is required.
Author contribution statement
DT designed the outline of the article, composed the manuscript and figures. MS provided scientific feedback and critical comments and revised content. Both authors read and approved the manuscript.
Financial support from the Ministry of Education, Youth and Sport of the Czech Republic through the National Program of Sustainability (Grant No. LO 1204) is gratefully acknowledged. The authors would like to also express thanks to Sees-editing Ltd., Prof. Claus Wasternack and Dr. Juraj Harmatha for their critical reading and editing of the manuscript.
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