Estrogens and Androgens in Plants: Comparison
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Please note this is a comparison between Version 2 by Peter Tang and Version 1 by Anna Janeczko.

Steroids are a group of compounds to which a number of crucial metabolism-controlling hormones belong. The group of steroid hormones that are present and active in animals and humans (mammalian steroid hormones) is large and includes, among others, corticosteroids, which control, for example, water and mineral management and sex hormones—i.e., androgens, estrogens, progesterone, which are responsible for development and reproduction.  Ecdysteroids are mainly known as being the steroid hormones of arthropods that regulate ecdysis and development. In plants, the steroid regulators include the brassinosteroids, which are hormones that have a multidirectional activity and are engaged in plant growth, development, and its response to environmental stresses.

  • testosterone
  • androsterone
  • androstenedione
  • estradiol
  • estrone
  • plants

1. Introduction—Steroid Hormones in Living Organisms

Steroids are a group of compounds to which a number of crucial metabolism-controlling hormones belong. The group of steroid hormones that are present and active in animals and humans (mammalian steroid hormones) is large and includes, among others, corticosteroids, which control, for example, water and mineral management and sex hormones—i.e., androgens, estrogens, progesterone, which are responsible for development and reproduction [1,2,3][1][2][3]. On the other hand, ecdysteroids are mainly known as being the steroid hormones of arthropods that regulate ecdysis and development [4]. In plants, the steroid regulators include the brassinosteroids, which are hormones that have a multidirectional activity and are engaged in plant growth, development, and its response to environmental stresses [5,6][5][6]. Interestingly, however, mammalian steroid hormones are also part of the metabolic profile in plants [7,8][7][8]. While the debate about whether these compounds are also hormones for plants is still open, currently, there is a great deal of literature data to show that mammalian steroids influence the physiological processes of plants. There are review articles devoted to this issue that are available, starting from older ones such as Heftmann [9], Geuns [10], Hewitt et al. [11] to newer ones such as Janeczko and Skoczowski [12], Speranza [13], or Islam [14].
The androgens and estrogens in mammals are synthesised from cholesterol [26][15] via pregnenolone and progesterone and are built based on an androstane or estrane skeleton, respectively (Figure 1). Among androgens, the most well-known compound is testosterone. This group also includes 5α-dihydrotestosterone (DHT), androsterone, dehydroepiandrosterone (DHEA), and 4-androstene-3,17-dione (androstenedione). Androsterone and testosterone in animals and humans are the main precursors of another group of hormones—estrogens—and enzyme aromatase also participates in this biosynthesis, which is also called estrogen synthetase/synthase. Estrogens include 17β-estradiol, estrone, and estriol. The chemical structure of selected androgens and estrogens is presented in Figure 1. The biosynthetic pathway of steroid hormones (androstane and estrane derivatives), presented in Figure 1, is well characterised in animals and humans. We can only suspect that a similar pathway also functions in plants.
/media/item_content/202201/61dd2294a616aplants-10-02783-g001.png
Figure 1. (A) A simplified model of the biosynthesis of steroid hormones (androstane and estrane derivatives) in animals and humans; (B) the chemical structure of androstane and selected androgens; (C) the chemical structure of estrane and the most important estrogens.

2. The Presence of Estrogens and Androgens in Plants: The Effect of Plant Growth Conditions and Plant Developmental Stage on the Steroid Content

According to the older literature data, estrogens were first found in plants as early as the 1930s [27][16], and then, for several decades, further studies documenting the presence of estrogens (and androgens) in plants were undertaken (reviewed in [12]). The development of analytical techniques in the last two decades has improved the detection of androgens and estrogens in plant material. This applies to improvements in methods of extraction and purification of compounds isolated from plant material (for example, the use of immunoaffinity columns with antibodies [28][17]), as well as detection methods (UHPLC–MS/MS and GC–MS/MS) [28,29,30][17][18][19]. There is also the possibility of using commercial kits for determining these compounds [31,32][20][21]. The presence of endogenous estrogens and androgens might be questioned, one reason of which is that these compounds are present in very small amounts, and at the same time, there are many other metabolic components in the plant extract that can hinder analysis and lead to false results. For this reason, in more advanced analytical methods, the step of appropriate cleaning of the sample should be emphasised. In the work of Simerský et al. [28][17], the sensitivity of the analysis is enhanced by including an immunoaffinity chromatography purification (using generic anti-Δ4-3-ketosteroid antibodies). These antibodies were used in the preparation of immunoaffinity gels for the purification and preconcentration of steroids in extracts. The use of immunoaffinity columns improved the sensitivity of UHPLC-ESI(+)-MS/MS measurement, and the so-called sample matrix effect was reduced and signal strength improved. In multiple-reaction-monitoring (MRM) mode, the detection limit for steroids was close to 10 fmol, and the response was linear up to 50 pmol injected. The MRM transitions from [M + H]+ ion to appropriate product ion provided precise quantification of the analysed steroids. The second MRM transition was also measured for each analyte to enable steroid conformation to be determined. The calculated MRM ratio was useful as another criterion based on which an analyte may be distinguished from interfering substances. More details about the procedure can be found in [28][17].
During the last 20 years, several papers that documented the occurrence of androgens and estrogens have been published. The compounds in question are present in plants at the pg and ng levels. The impact of plant growth conditions and the plant developmental stage on the steroid content was also confirmed. In some cases, it has even been possible to correlate the changes in the concentration of estrogens and androgens with specific physiological processes.

3. Physiological Activity of Estrogens and Androgens in Plants

3.1. Plant Growth and Reproduction

3.1.1. Plant Growth

The impact of estrogens and androgens on plant growth was already described in the first half of the 20th century (reviewed by [12]). In the last 20 years, few new works have been published that describe the effects of these hormones on plant growth, development, or other processes, as well as revealing some of the mechanisms of their action in detail. Interestingly, however, in recent years, there has been a number of works that have been devoted to the study of the impact of these mammalian hormones on plants due to the fact that they are found in waste or sewage and thus are ‘artificially’ introduced into the environment [41,42,43,44][22][23][24][25]. In these works, the authors show that high concentrations of estrogens have a harmful effect on plant growth, morphology, and development. According to Adeel et al. [44][25], in lettuce, the application of estrogen (17β-estradiol 10 mg/L) significantly reduced the total root growth and development, which was connected to an increased accumulation of H2O2, higher lipid peroxidation, and a higher activity of the antioxidant enzymes. Moreover, 17β-estradiol (at the same concentration), when applied to corn, inhibited kernel germination and corn seedling growth [43][24]. The studies of Brown [42][23] were devoted to determining the effects of mammalian estrogens (17β-estradiol, estrone, and estriol) on the growth and tuberisation of potato plants (Solanum tuberosum L.). At a concentration of as low as 0.1 mg/L, estrogen reduced root growth, while 10 mg/L of estrogen caused plant deformities and induced a callus. Tuber production was slightly lower in the plants to which estrogen had been applied, compared with the control. Estrogens at a concentration of 10 mg/L also lowered the activity of an enzyme (acid phosphatase) that is important in plant mineral management, etc.
Although these reports proved that at high concentrations, estrogens have an inhibitory effect on the growth processes in plants, simultaneously, at lower concentrations, they might have a biostimulative effect on metabolism. In lettuce, estrogens that were applied at concentrations of 0.1–50 µg/L enhanced the photosynthetic pigments, root growth, and shoot biomass [44][25]. In addition, 17β-estradiol (10−6 M) stimulated the accumulation of the photosynthetic pigments in Wolffia arrhizal [41][22]. Dumlupinar et al. [45][26] found that a 10−6 M concentration of 17β-estradiol and androsterone, when applied to seven-day-old barley seedlings via spraying, increased the concentrations of calcium, magnesium, phosphorus, sulphur, copper, manganese, aluminium, zinc, iron, potassium and chlorine most effectively, while they decreased the sodium concentration in barley leaves (measured 18 days after spraying). Further, 17β-estradiol (at a concentration of 0.1 mg/L) stimulated germination and seedling growth in corn [43][24]. According to Brown [42][23], however, even at 0.1 mg/L, estrogens reduced root growth in potato plants although the acid phosphatase activity of the plants increased. In chickpea (Cicer arietinum) plants, a concentration of 17β-estradiol and androsterone 10−9 M (applied to seven-day-old plants) was the most active in stimulating plant growth, which was connected with an increased protein and sugar content 18 days after spraying [46][27]. The contents of mineral elements such as K, S, Na, Ca, Mg, Zn, Fe, P, Cu, and Ni were higher, whereas Mn and Cl were lower [47][28]. The same concentration of these steroids also effectively lowered the H2O2 content and lipid peroxidation along with a higher activity of the antioxidative enzymes [46][27]. Erdal and Dumlupinar [48][29] studied also the effects of 17β-estradiol on germination, root and shoot growth, and the biochemical background (among the other activity of α-amylase) in chickpea. The seeds, which had been germinated at a few concentrations of steroid from 10−4 to 10−15 M were then analysed at the end of the 1st, 3rd, and 5th days. Based on the results, 17β-estradiol accelerated seed germination at the end of days 1 and 3, and the root, and shoot growth was also stimulated. The most effective concentrations of 17β-estradiol were in the range of 10−9–10−12 M. These effects were accompanied by an increase in the activity of α-amylase during germination. The effect of 17β-estradiol, estrone, and androsterone on the in vitro regeneration of Triticale mature embryos was described by Uysal and Bezirganoglu [49][30]. Estrogens had the best result on the percentage of explants that formed shoots.

3.1.2. Plant Reproduction

The impact of estrogens and androgens on plant development (some aspects such as sex expression) was described before 2000 (reviewed in [12]). The regulatory effect of estrogens and androgens on sex expression in plants was, however, also critically reviewed by Jones and Roddick [50][31]. In the last 20 years of studies, this aspect of steroid activity was rather abandoned and other effects of steroids on generative development were emphasised.
In some ornamental plants (Petunia hybrida, Tagetes erecta, and Calendula officinalis), 17β-estradiol (1 mg/L) increased the leaf area but not the flowering longevity [51][32]. Żabicki et al. [52][33], on the other hand, studied the effect of estrone (1 and 3.7 µM) on the differentiation of the somatic tissues and on the induction of an autonomous endosperm in a culture of female gametophyte cells of Arabidopsis thaliana. Estrone stimulated the development of an autonomous endosperm in unpollinated pistils, direct organogenesis, callus proliferation, and the formation of trichome-like structures (‘hairs’). Histological analysis revealed adventitious root formation. Rojek et al. [53][34] examined the effect of exogenous estrone and androsterone on an unfertilised egg and central cell divisions in a culture of unpollinated pistils of A. thaliana wild-type and fie mutants. Both steroids stimulated the central cell divisions and fertilisation-independent endosperm development. The stages of autonomous endosperm development were similar to the pattern that was observed after fertilisation. Importantly, the developmental arrest of the autonomous endosperm at the nuclear stage was overcome by the application of the steroid, as the switch from the nuclear to the cellular stage of the endosperm is required for the correct embryo and seed development. In the fie mutants, which inherited the autonomous underdeveloped endosperm (more about fie in [54][35]), the steroids clearly accelerated and promoted the development of the full fie autonomous endosperm. The changes in the methylation of the FIE gene (FERTILIZATION-INDEPENDENT ENDOSPERM gene; [54][35]) were established in in vitro conditions [53][34], which suggests that full autonomous endosperm development could be a synergistic effect of changes in the histone modification and DNA methylation within a distinct set of common target genes that are involved in endosperm development [53,55,56][34][36][37].
The effect of estrogens (estrone, estriol, 17β-estradiol) and androgens (androsterone, androstenedione) on the generative induction of A. thaliana and winter wheat was described by Janeczko and Filek [57][38] and Janeczko et al. [58][39]. A. thaliana is a plant with a photoperiodical flowering control (it needs long-day conditions to induce a bloom). Winter wheat (especially the cultivar Grana), on the other hand, has a thermoperiodical control of development, which means that it needs a sufficiently long cold period (usually a few weeks) to induce the generative stage. In the case of both species, failure to meet these conditions (or their fulfilment in an incomplete manner, for example, too short of a cold period for wheat) results in generative developmental disorders, delayed flowering, or even suppressed flowering. Hence, both plants are useful models to study the activity of the regulatory compounds in relation to the stimulation of generative development because it can be determined whether they replace the action of the physical factors such as the length of the day (A. thaliana) or the cold period (winter wheat). Janeczko et al. [58][39] found that A. thaliana responded (in relation to the induction of generative development) to the application of estrogens and androgens differently in vitro. The absolute control plants (grown under long-day conditions throughout the growing season) reached a 100% generative phase. Only 41 percent of the plants that were only allowed 7 days of growth under long-day conditions (second control) reached the generative phase. Androsterone and androstenedione (at a concentration of 0.1 μM), when applied in the same growth conditions as the second control, had the opposite effect on the generative development of A. thaliana than the estrogens did. The androgens increased the percentage of generative plants up to 90–96%, respectively (almost to the level noted in the absolute control). The estrogens at the same concentration decreased the number of generative plants to as little as 0 (in the case of estrone). On the other hand, a higher concentration (1 µM) of estrone increased the percentage of plants in the generative stage by up to 80%, 17β-estradiol by almost up to 70%, while estriol yielded results that were similar to the second control. Androgens at a concentration of 1 µM also stimulated generative development; however, in the case of androsterone, it was less effective than at a concentration of 0.1 µM.
To summarise, experiments using exogenous estrogens and androgens have shown a wide spectrum of their effects on plant growth and development. Unfortunately, it is currently not possible to confirm the physiological activity of estrogens and androgens in plants in tests on mutants with disturbances in the biosynthesis of these compounds (such mutants are not available to the best of the author’s knowledge). However, an alternative (and chance) is to use the inhibitors of androgen/estrogen biosynthesis implemented from medical sciences, as was carried out in the case of progesterone [59][40].

3.2. Plant Stress Response

Compared with the studies on the activity of estrogens and androgens on the growth and development of plants, which, as was mentioned above, had already begun in the first half of the 20th century, research on the anti-stress activity of these compounds has mainly been performed in the last 20 years. One of the reasons for this is the fact that during this period, the general research interest in the mechanisms of the plant stress response increased. During their growth in the environment, plants are exposed to many stress factors—abiotic (a deficit or excess of water, a too low or high temperature, salinity, heavy metals) and biotic (pathogens). Their impact on plant yield has become more and more important from an economic point of view in light of the increasing world population. Many researchers are searching for/studying the antistress-protecting regulators that might alleviate plant stress. For steroids, these studies are mainly focused on the plant hormones, brassinosteroids (extensive literature is available), although mammalian steroid hormones have also been of research interest. The effects of estrogens/androgens on the metabolism of crop plants (mainly from the cereal group and from the Fabaceae family), under low-temperature stress, drought, salinity stress, and heavy metal stress have been studied [15,38,60,61,62,63][41][42][43][44][45][46].

4. Transport and Conversion of Estrogens and Androgens in Plants

Important elements of the physiological activity of various regulators are their uptake and accumulation in plant tissues. The research that has been conducted to date, which has shown that estrogens and androgens can be absorbed by plants, was conducted mainly because the environment may be contaminated with these compounds (animal-based waste, manure). Nevertheless, they provided information that plants are able to uptake steroids, and their accumulation (greater or lesser) influences the physiological processes in a dose-dependent manner [44][25]. The uptake of 17α-ethynylestradiol in bean plants (Phaseolus vulgaris) was confirmed by Karnjanapiboonwong et al. [72][47]. An accumulation of 17α-ethynylestradiol was detected in the roots and leaves. In plants that were grown in sand (conditions of high contaminant bioavailability), the accumulation was higher than in plants that were grown in soil. The shoots and roots of maize that had been exposed to hydroponic solutions containing 2 μM 17β-estradiol and estrone also accumulated these compounds [73][48]. Estrogens were found in the roots at concentrations of up to 0.19 μmol/g; the highest level was after 1–3 days of exposure. Only 17β-estradiol was accumulated in the shoots. The authors also suspected a transformation and/or irreversible binding processes of estrogens in plant tissues. In another study, [74][49] proved oxidative (17β-estradiol to estrone) and reductive (estrone to 17β-estradiol) transformations. The combined effects of plant enzymes and plant-associated microbes were responsible for those transformations. The uptake and possibilities of converting estrogens were also studied in a culture of lettuce [44][25]. Two estrogens—17β-estradiol and ethinyl estradiol—were administrated to plants at concentrations of 0, 0.1, 50, 150, 2000, and 10,000 µg/L via the roots (nutrient medium). The uptake was dose dependent, and a higher level of the applied estrogens was detected in the leaves and roots. In control plants, estrogens were not found. Biotransformation of applied estrogens was noted. In the case of the roots of lettuce, after the application of 17β-estradiol (lower concentration), estrone was also detected. The application of higher concentrations of 17β-estradiol also resulted in an accumulation estrone and 17α-estradiol. In the case of the leaves, both compounds were detected no matter which concentration was applied. After the application of ethinyl estradiol in the roots and leaves (especially when a higher concentration was used) ethinyl estradiol as well as estrone, 17β-estradiol, and 17α-estradiol were detected.
As for the androgens, data are available for 17β-trenbolone. Trenbolone belongs to synthetic androgens that have anabolic properties. Blackwell et al. [75][50] described the uptake and biotransformation of 17β-trenbolone in Phaseolus vulgaris. In this study, 17β-trenbolone was biodegraded to trendione (less active androgen) in vegetated sands (microbial degradation). In plants, the trenbolone metabolites were primarily concentrated in the roots, and only small concentrations were moved to stem and leaves.
To conclude, plants are able to uptake/transform estrogens and androgens. The microbial enzymatic systems also participate in the biotransformations of estrogens and androgens [74,75][49][50].

5. Receptors (Specific Binding Sites) of Estrogens and Androgens in Plants

Estrogen and androgen receptors in animals and humans are well known and described, although new discoveries are still being made in this regard. It can generally be assumed that there are three groups of these receptors—membrane, nuclear, and cytoplasmic [76,77,78,79,80,81][51][52][53][54][55][56].
To date, the knowledge about the putative estrogen receptors in plants is very limited, although it seems that a similar division of estrogen-binding proteins (membrane, nuclear, and cytoplasmic) also exists in the plant kingdom. In plants, Milanesi et al. [36][57] and Milanesi and Boland [37][58] described the presence of putative estrogen receptors (estrogen-binding sites) in Solanum glaucophyllum and Lycopersicon esculentum. Experiments were performed using [3H]17β-estradiol. The S. glaucophyllum callus also contained (except for the natural estrogens) estrogen-binding sites [36][57]. More in-depth studies showed that the estradiol-binding capacity can be found in the soluble fractions of the roots, stems, and leaves of S. glaucophyllum and L. esculentum. The range was from 100 to more than 3000 fmol/mg of protein and was dependent on the organ (the highest was in roots, and the lowest was in leaves). Western and ligand blot analyses suggested that the estrogen-binding proteins in plants may be present in a nuclear fraction, mitochondrial fraction, microsomes, and cytosol [37][58]. The presence of specific binding sites in the cytosol and membrane fraction was also described by Janeczko et al. [82][59] for winter wheat (up to more than 40 fmol/mg protein). The membrane and cytosol fractions of non-vernalised (control) and vernalized (cold-treated) plants were tested using a tritium-labelled ligand. The specific binding of [3H]17β-estradiol was detected, and it was generally higher in the membranes than in the cytosolic fraction. The specific binding of ligand was dependent on the plant growth conditions and was higher in the membrane fraction in the control than in the cold-exposed plants. Due to the positive effect of estrogens on stimulating the development of winter wheat [57][38], it is likely that these specific binding sites of 17β-estradiol are engaged in the mechanism of wheat development, but this will require further studies.

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