The presence and activity of progesterone in the plant kingdom

The presence and activity of progesterone in the plant kingdom

Steroids 77 (2012) 169–173 Contents lists available at SciVerse ScienceDirect Steroids journal homepage: www.elsevier.com/locate/steroids Review T...

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Steroids 77 (2012) 169–173

Contents lists available at SciVerse ScienceDirect

Steroids journal homepage: www.elsevier.com/locate/steroids

Review

The presence and activity of progesterone in the plant kingdom Anna Janeczko ⇑ Institute of Plant Physiology, Polish Academy of Sciences, Niezapominajek 21, 30-239 Krakow, Poland

a r t i c l e

i n f o

Article history: Received 9 September 2011 Received in revised form 26 October 2011 Accepted 27 October 2011 Available online 6 November 2011 Keywords: Progesterone Plants Presence Activity Receptors

a b s t r a c t Steroids are present in living organisms as one of the most essential groups of compounds. Continuous research has led to new discoveries and the revision of existing information concerning the occurrence and the role of steroids, both in animals and plants. This article will focus on reviewing the literature studying progesterone in the plant kingdom, including its discovery, its occurrence in different plant species as well as its biological activity and molecular basis of action. This review will present and discuss the current data in addition to introducing potential directions for further research on the subject of progesterone in plants. Ó 2011 Elsevier Inc. All rights reserved.

Contents 1. 2. 3. 4. 5. 6. 7.

Introduction: steroid compounds in living organisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The structure, activity and level of progesterone in mammals . . . . . . . . . . . . . . . . . . . . . . . . The discovery and presence of progesterone in plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The metabolism of progesterone in plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The activity of progesterone in plants: impact on the growth, flowering and other effects . Plant receptors of progesterone and their molecular mechanism of action . . . . . . . . . . . . . . Concluding remarks - is progesterone a plant hormone candidate?. . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction: steroid compounds in living organisms Steroids are present in living organisms as one of the most essential groups of compounds, and they are structurally derived from the sterane skeleton. The term ‘‘steroids’’ was first used by Callow in 1936 for the ‘‘group of compounds comprising the sterols, bile acids, heart poisons, saponins and sex hormones’’ [1]. The present-day classes within the steroid group include: brassinosteroids, ecdysteroids, cucurbitacins, cardenolides, mammalian steroid hormones, sterols, bufadienolides, withanolides, steroid alkaloids, sapogenis and bile acids. Some of these compounds, like sterols, are common in both the plant and animal kingdom, serving as membrane components or as precursors for other steroids. Other compounds are limited to one or only a few plant families,

⇑ Tel.: +48 12 425 18 33; fax: +48 12 425 18 44. E-mail address: [email protected] 0039-128X/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.steroids.2011.10.012

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such as the cucurbitacins found in Cucurbitaceae or the cardenolides present in Scrophulariaceae. A large of number of steroid groups possess regulatory (hormonal) properties. Brassinosteroids are known to be plant hormones, while ecdysteroids are insect hormones. The mammalian steroid hormones (corticoids, estrogens, androgens and progesterone) are crucial for cell metabolism and mammal reproduction. Continuous research has led to new discoveries and the revision of existing information concerning the occurrence and role of steroids, both in animals and plants. Some good examples of the new discoveries can be gleaned from the findings concerning the function of progesterone in mammals and especially in plants. This article focuses on reviewing the literature on progesterone in the plant kingdom, including its discovery, its occurrence in different plant species as well as its biological activity and molecular basis of action. The aim of this review is to present and discuss the current data in addition to introducing potential directions for further research on the subject of progesterone in plants.

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Fig. 1. (A) Biosynthesis of progesterone in the caredenolide-producing plant Digitalis lanata Ehrh. [18,19]. (B) Conversion of exogenously applied progesterone in a cell culture of Nicotiana tabacum L. and Sophora angustifolia L. [10]. (C) Comparison of the structure of the plant membrane steroid binding protein (isolated from Arabidopsis) and human progesterone receptor (PGC2). The marked numbers belong to the amino acids based on [41].

2. The structure, activity and level of progesterone in mammals Progesterone (PROG) is a C-21 steroid (pregn-4-ene-3,20-dione; Fig. 1A and B). Progesterone was discovered in the corpus luteum of mammals and was first chemically synthesized at the beginning

of the XX century. In humans, this steroid regulates the course of pregnancy and, together with estrogen, regulates menstruation [2]. Additionally, it is a precursor to androgen and estrogen biosynthesis. PROG is also a neurosteroid important for brain functioning [2]. Daily production of progesterone (lg d 1) averages 150 in boys,

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250 in girls, 420 in men and up to 19,600 in women [3]. The average concentrations of serum progesterone are 0.38–1.0 nmol dm 3 for men and 0.06–95 nmol dm 3 for women.

3. The discovery and presence of progesterone in plants The presence of progesterone in plants was first reported in the 1960’s by Gawienowski and Gibbs [4]. They estimated the amount of PROG in 500 ng g 1 of apple seeds using the thin layer- and gaschromatography methods. Simons and Grinwich [5] later noted the presence of PROG in a range of plant species (80% of plants from 50 families) using radioimmunoassay (RIA) where ethanol extracts of plant tissues were analyzed without purification. Interestingly, Simons and Grinwich noticed that progesterone levels not only varied between different species but also between different organs (generative or vegetative). They also suggested that progesterone levels could be dependent on certain physiological processes and steroid functions. For example, the concentration of PROG in the leaves of Prunus virginiana L. was found to be 13 ng g 1 of dry weight. In the flower buds, the concentration increased to 58 ng, but then in the flowers it again decreased to 7 ng. In 1998, Hartmann et al. measured the concentration of steroid hormones (including progesterone) in food using a gas-chromatography/ mass spectrometry (GC–MS) method [3]. Progesterone was found in the more obvious products of animal origin, such as meat and eggs, but also in steamed potatoes (5.07 ng g 1), wheat meal (up to 2.86 ng g 1), parboiled rice (0.38 ng g 1), natural olive oil (0.08 ng g 1) and refined corn oil (0.31 ng g 1). Using GC–MS, Iino et al. [6] identified and quantified progesterone in seven dicotyledons and two monocotyledons. Their work confirmed the earlier finding of Simons and Grinwich that the progesterone concentration changes according to a plant organ’s dependency. Iino et al. reported, for the first time, the presence of PROG in the model plant Arabidopsis thaliana L. The steroid was found in the shoots and inflorescences with concentrations of 160 and 400 ng kg 1 of fresh weight, respectively. In 2008, Carson et al. conducted studies with unexpected results [7]. Progesterone and androgens were previously identified in the water and sediment of a river in Florida, USA, in which masculinized female mosquitofish were found downstream from a paper mill. Using liquid-chromatography/mass spectrometry, PROG was detected in the mature pine wood, needles and bark that were present in the paper pulp. The pulp had been dumped into the water where it became the precursor for androgens in the environment [7]. This phenomenon of hormonal pollution was also observed in other rivers and is discussed in the article ‘‘Macho Waters’’ [8]. Simersky´ et al. have developed the most sophisticated method for estimating PROG in plant material [9]. They detected the presence of PROG in three tested species: Nicotiana tabacum L. (55.46 pmol g 1), Digitalis purpurea (58.92 pmol g 1) and Inula helenium L. (2.10 pmol g 1). Along with other methods, Simersky´ et al. used specially prepared columns with antibodies selectively binding progesterone to purify the plant extract. The presence of the steroid was then confirmed using ultra performance liquid chromatography tandem mass spectrometry (UPLC-MS/MS) [9]. The above data describe the occurrence of free progesterone in plant cells. In animals, steroid hormones – as hydrophobic molecules – are present and transported in conjugates with proteins or as their glucuronide and sulfate forms. PROG conjugates were found in plant cell suspensions as a product of the conversion of exogenously applied labeled progesterone [10,11]. According to the preliminary data obtained by Janeczko et al. in 2011, progesterone is naturally present in wheat seedlings in its conjugate form (as glycosides) [12]. Using the method of Simersky´ et al., the authors performed enzymatic hydrolysis of plant extracts using

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one of glycosidases (b-glucuronidase, type HP-2:, from Helix pomatia) to estimate PROG content [9]. In this study, the estimated amount of progesterone in the hydrolyzed extract was four times higher (2.29 pmol g 1 of fresh weight) than in the untreated extract (0.55 pmol) ([12], author unpublished data). The presence of the conjugated forms of progesterone in plants still requires additional study. 4. The metabolism of progesterone in plants The study of the metabolism of progesterone began in the late 1960’s. Researchers in this field have focused their work on the following plants: D. purpurea L. [11,13,14], Digitalis lanata Ehrh. (Scrophulariaceae) [15–19], N. tabacum L. (Solanaceae) [10,20,21], Sophora angustifolia L. (Phabaceae) [10], Dioscorea deltoidea Wall. ex Kunth (Dioscoreaceae) [22], Holarrhena floribunda (Don) T. Durand and Schinz [23], Cheiranthus cheiri (L.) Crantz (Brassicaceae) [24] and Chlorella emersonii C211-8H (green alga) [25]. The problem of the metabolism of progesterone by plant cell tissues is well discussed in the review article by Stohs and Rosenberg [26]. Investigations were based on the application of labeled sterols, pregnenolone or progesterone to plant cell suspension cultures and to whole plants. The metabolites isolated from the treated suspensions were then analyzed. Summarizing the work, it can be said that (1) the sterol precursors of progesterone in plants may be cholesterol, campeserol, sitosterol and stigmasterol; (2) pregnenolone is intermediate in the progesterone pathway of biosynthesis; and (3) the progesterone in plant cells may be converted into pregnane derivatives and their conjugates (fatty acids or glycosides). A schematic diagram of the biosynthesis of progesterone is presented in Fig. 1A for D. lanata Ehrh., which is a cardenolide-accumulating plant [18]. The mechanism is presented together with a depiction of the possible conversion of exogenously applied progesterone to 5a-pregnanolone palmitate (Fig. 1B), as described by Furuya et al., in the cell culture of N. tabacum L. and S. angustifolia L. [10]. 5. The activity of progesterone in plants: impact on the growth, flowering and other effects In animals and humans, PROG is primarily involved in the female menstrual cycle, pregnancy and embryogenesis regulation. Consequently, PROG was assumed to function as a plant growth and development regulator in most of the research concerning the activity of progesterone in plants. Studies on sunflowers showed that depending upon the applied concentration, progesterone promoted or inhibited the growth of sunflower shoots and roots [27]. High PROG concentration (0.25 lg per plant) stimulated the elongation of shoots, while a lower concentration (0.1 lg per plant) stimulated the growth of sunflower roots. A 1-lM concentration of progesterone applied to in vitro wheat seedlings stimulated the growth of leaves and roots but inhibited such growth when applied in concentrations 10 times higher [28]. Iino et al. tested a wider range of PROG concentrations in an A. thaliana culture [6]. They found a slight stimulation of seedling growth on media containing 0.01–1 lM of PROG, while a steroid concentration of 100 lM had an inhibitory effect on growth. The surprising result was that progesterone promoted the growth of the gibberellin-deficient pea mutant (lh) but not the brassinosteroid-deficient pea mutant (lkb) [6]. According to Iino et al., plant response to progesterone may be somehow connected with the metabolism of the gibberellins. Moreover, PROG increases the amount of mineral components (calcium, magnesium, phosphorus and sulfur) that are necessary for the growth processes in plants. Such findings demonstrate PROG’s influence on plant mineral management [29,30]. The mineral uptake effect was also observed by Kirkham

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in experiments where wheat was treated with norethindrone [31]. Norethindrone is a synthetic hormone that is similar in structure and function to naturally produced progesterone and is used as a drug to treat certain female reproductive tract disorders. In terms of promoting plant growth, progesterone also stimulates the tube growth of in vitro mature tobacco pollen [32]. This finding further points to the work of Speranza et al., who detected increasing amounts of PROG (and other steroid hormones) during the germination of kiwifruit pollen [33]. Finally, progesterone induces the plant flowering of winter wheat (concentrations of 1 and 10 lM) and A. thaliana L. (concentration of 1 lM) [34,35]. In this case, PROG application partially replaces the necessity of exposing plants to a long photoperiod (Arabidopsis) or cold treatment (winter wheat), which is normally required for the correct development of both plants. In wheat, PROG stimulated generative development by increasing the percentage of heading plants and accelerating the heading [34]. It is worth noting that transgenic tobacco plants carrying the CYP11A1 cDNA, encoding cytochrome P450SCC (responsible for the conversion of cholesterol into pregnenolone) from the bovine adrenal cortex, showed increased flowering when compared to the wild type plants [21]. These transgenic tobacco plants were also characterized by early flowering, and increased amounts of pregnenolone and progesterone were found in the leaves [21]. More recently, studies have shown that progesterone in chickpea plants stimulates the activity of anti-oxidative enzymes such as catalase [36]. Such activity points to the potential role of PROG in response to certain environmental biotic or abiotic stressors. Our own research has shown the protective effect of PROG on the membrane permeability and photosystem II efficiency of A. thaliana L. infected with Pseudomonas bacteria (author’s unpublished data). This review shows that the activity of exogenous progesterone in plants appears to be multidirectional. There are undoubtedly many unknown processes sensitive to PROG. Several of the findings concerning progesterone may be useful in practice (i.e., for stimulation of flowering in ornamental plants); however, evaluating the real significance of progesterone for plant development points to further studies involving specially designed experiments, such as with the use of progesterone biosynthesis inhibitors.

6. Plant receptors of progesterone and their molecular mechanism of action An important part of hormone action is its perception in plant cells. Plants perceive hormones through specific protein-receptors. Much is known about the perception of steroid hormones in animal and human cells, and generally, there exist two possible mechanisms of steroid action: slow genomic response, where the involved receptors are located in the cytoplasm or nucleus, and rapid non-genomic response mediated by membrane receptors [37]. Much less is known about the perception of steroid regulators in plants. The only commonly accepted hormones of a steroid nature in the plant kingdom are brassinosteroids. According to present knowledge, this family of hormones has receptors within the cell membrane [38–40]. Recently, molecular studies revealed the presence of progesterone binding sites (putative receptors) in the plant cell membrane and in the cytosolic fraction [41,42]. Yang et al. [41] identified a membrane steroid binding protein (MSBP1) in A. thaliana (Fig. 1C). The MSBP1 gene encodes a 220-amino acid protein that can bind to progesterone (high affinity) and other steroids (5-dihydrotestosterone, 24-epibrassinolide; low affinity). MSBP1 functions as a negative regulator of cell elongation. Transgenic plants overexpressing the MSBP1 gene have a short hypocotyl and a higher steroid binding capacity in the membrane fractions. Antisense MSBP1 transgenic plants have a long hypocotyl and

reduced steroid binding capacity. Researchers postulate that membrane steroid proteins bind cell elongation–stimulating steroids, thus preventing binding to their action site. The result is suppressed cell elongation. The observed response of the MSBP1-overexpressing and the antisense-MSBP1 plants to exogenously applied steroid supports the hypothesis of Yang et al. MSBP1-overexpressing plants showed a reduced response to exogenous steroid treatment, while antisense-MSBP1 plants were hypersensitive. Expression of MSBP1 in the Arabidopsis hypocotyl was suppressed under dark conditions and activated by light. This action suggests that MSBP1 plays a role in the light inhibition of hypocotyl elongation. Recently, it has been shown that MSBP1 is involved in auxin redistribution and regulates tropism in Arabidopsis [43]. MSBP1 can also participate in the signaling of brassinosteroids [44]. According to Iino et al., the genes encoding putative progesterone-binding proteins are also present in rice (OsMSBP1,2) [6]. Based on the available plant Expressed Sequence Tag data, it has been hypothesized that progesterone-binding membrane proteins should be present in various plant species. Janeczko et al. reported the presence of specific binding sites for progesterone in wheat leaves [42]. Using radioligand binding analysis, they identified binding sites located within the cytoplasm and cell membrane. These site numbers changed as a result of cold treatment (vernalization). In the cytoplasm, the number of specific binding sites increased as a result of vernalization, while the number of binding sites located in the cell membrane decreased. Changes in the number of potential progesterone receptors may be part of the mechanism regulating the process of vernalization and other physiological processes in plants. The study of progesterone perception adds new data to the available information on the mechanisms of steroid regulators in plants. The data suggest that in plants as well as animals, there may only be a few kinds of steroid binding receptors that are located within various organelles within the cell.

7. Concluding remarks - is progesterone a plant hormone candidate? The study of progesterone occurrence, activity and mechanism of action has been given less attention than studies on brassinosteroids. Brassinosteroids are a group of steroids that have regulatory properties in plants. They have been hailed as hormones on the basis of widespread attention and study. This article, however, provides a broad selection of collected and reviewed data that are sufficient for discussing whether progesterone is a plant hormone candidate. According to its definition, a plant hormone is a ‘‘naturally occurring, organic substance which at low concentrations influences physiological processes’’ [45]. In this basic definition, the following two essential points are not explicitly stated: (1) that a hormonal compound should be universally present in all plants and (2) that its action in plants cannot be trophic. Progesterone, as a steroid compound, does not have a trophic nature. The amounts of progesterone in the tissues are, in fact, minimal. Nevertheless, still more research is needed, using accurate analytical methods, to prove the presence of PROG in a wider spectrum of plants. A technique used by Simersky´ et al. [9] is one of the most appropriate. Application-only immunoassay techniques (developed to analyze serum) rather should not be used in the case of crude plant extracts because of possible overestimation of steroid content. The use of mutants (i.e., with impaired biosynthesis of progesterone) or experiments using inhibitors of biosynthesis or PROG action must also be performed. Such experiments have already uncovered the mechanism, action and functions of the brassinosteroid compounds mentioned above [46]. In essence, Yang at al. [41], Iino et al. [6] and Spivak et al. [20,21] can be regarded as

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pioneers on the subject of progesterone, but the continuation of their work and the development of other approaches are needed. Based upon the information presented in this article, we can formulate the hypothesis that progesterone has a hormonal nature in plants, although additional studies are needed to verify this hypothesis.

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