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Year : 2015  |  Volume : 11  |  Issue : 42  |  Page : 225-230  

Phytoecdysteroids of the East Asian Caryophyllaceae

1 Laboratory of Plant Chemotaxonomy, G.B. Elyakov Pacific Institute of Bioorganic Chemistry of the Far Eastern Branch of the Russian Academy of Sciences, Vladivostok, Russia
2 Laboratory of Comparative Biochemistry, A.V. Zhirmunsky Institute of Marine Biology of the Far Eastern Branch of the Russian Academy of Sciences, Vladivostok, Russia
3 Far East Federal University, Vladivostok, Russia

Date of Submission13-Jan-2014
Date of Acceptance24-Feb-2014
Date of Web Publication27-May-2015

Correspondence Address:
Dr. Elena Novozhilova
Laboratory of Plant Chemotaxonomy, G.B. Elyakov Pacific Institute of Bioorganic Chemistry of the Far Eastern Branch of the Russian Academy of Sciences, 159 Prospect 100-let Vladivostoku, Vladivostok 690022
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0973-1296.157746

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Background: Occurrence of integristerone A (1), 20-hydroxyecdysone (2), ecdysone (3), 2-deoxy-20-hydroxyecdysone (4) has been analyzed in 64 species of the East Asian Caryophyllaceae. Materials and Methods: Ecdysteroid content was determinate by high-performance liquid chromatography (HPLC). HPLC with a high-resolution mass spectrometry was performed on Shimadzu LCMS-IT-TOF (Japan) system equipped with a LC-20A Prominence liquid chromatograph, a photodiode array detector SPD-M20A and ion-trap/time-of-flight mass spectrometer. Results: New sources of phytoecdysteroids: Melandrium sachalinense and Melandrium firmum have been revealed. It is the 1 st time that two has been identified in M. sachalinense and M. firmum; 1 in the species: Lychnis fulgens, Silene repens, Silene foliosa, Silene stenophylla, Silene jenisseensis and M. sachalinense; 3 in Lychnis cognata; 4 in L. fulgens, S. stenophylla and S. jenisseensis (the tribe Lychnideae, the subfamily Caryophylloideae). Ecdysteroid-negative taxa are Spergularia rubra of the tribe Sperguleae; species of the genera Minuartia, Honckenya, Eremogone, Arenaria, Moehringia, Pseudostellaria, Fimbripetalum, Stellaria and Cerastium of the tribe Alsineae; Scleranthus annuus of the tribe Sclerantheae, as well as the East Asian representatives of the genera Gypsophila, Psammophiliela, Dianthus and Saponaria of the tribe Diantheae; Oberna and Agrostemma of the tribe Lychnideae. Conclusion: This investigation shows the most promising sources of ecdysteriods are species of genera Silene and Lychnis.

Keywords: Caryophyllaceae, ecdysteroids, high-performance liquid chromatography

How to cite this article:
Novozhilova E, Rybin V, Gorovoy P, Gavrilenko I, Doudkin R. Phytoecdysteroids of the East Asian Caryophyllaceae. Phcog Mag 2015;11, Suppl S1:225-30

How to cite this URL:
Novozhilova E, Rybin V, Gorovoy P, Gavrilenko I, Doudkin R. Phytoecdysteroids of the East Asian Caryophyllaceae. Phcog Mag [serial online] 2015 [cited 2022 Dec 8];11, Suppl S1:225-30. Available from: http://www.phcog.com/text.asp?2015/11/42/225/157746

   Introduction Top

Plants of the family Caryophyllaceae are perspective sources of phytoecdysteroids-hormones which control molting in insects and crustaceans. Phytoecdysteroids possess stimulating and adaptogenic action, causing considerable decrease in cholesterol content in blood serum and displaying anabolic activity in relation to human and mammals; in this case, unlike anabolic steroids, ecdysteroids, possessing pronounced anabolic activity, do not manifest androgen effect to make possible their lengthy use. Their use in medicinal preparations of adaptogenic, cardiotropic, antiatherosclerotic, counter-ulcer, would-healing and antimicrobial action was shown to be promising. [1],[2],[3]

First studies on phytoecdysteroids of the Caryophyllaceae in the flora of the former Soviet Union were conducted by the researchers of the Institute of the Chemistry of Plant Substances of the Academy of Sciences of the Uzbek SSR (Tashkent city) in the 1980s. [4],[5],[6],[7],[8],[9]

New sources of phytoecdysteroids are actively sought. Distribution pattern of integristerone A (1), 20-hydroxyecdysone (2), ecdysone (3), 2-deoxy-20-hydroxyecdysone (4) in plants is studied. [10],[11],[12],[13]

   Materials and Methods Top


Standards of compounds 2, 3, and 4 were obtained from Sigma and Aldrich Company (St. Louis, MO, USA). Compound 1 was obtained from U. A. Baltaev (Institute of Petroleum Chemistry and Catalysis, Ufa, Russian Federation). All solvents and chemicals were of analytical grade.

Plant materials

The plant material from wild flora was collected during 2005-2012 years in the Far East, Russian Federation. Specimens have been deposited in the herbarium of the laboratory of plant chemotaxonomy of G. B. Elyakov Pacific Institute of Bioorganic Chemistry of the Far-Eastern Branch of the Russian Academy of Sciences. Ecdysteroid content was analyzed in the aerial part of plants collected during their flowering period.

Analysis of ecdysteroids

Air-dried samples (about 200 mg, accurately weighed, residual moisture <8.2%) were extracted with ethanol-water (7:3, 10 mL) at room temperature for 3 days. The resulting extracts were filtered. A portion (0.9 mL) was treated with water (12 mL). Solid-phase extraction was carried out with Supelclean C18 columns (Supelco, St. Louis, USA) using ethanol-water (3:2) as eluent.

High-performance liquid chromatography (HPLC) with a high-resolution mass spectrometry was performed on LCMS-IT-TOF (Shimadzu, Kyoto, Japan) system equipped with a LC-20A Prominence liquid chromatograph, a photodiode array detector SPD-M20A (Shimadzu, Kyoto, Japan) and ion-trap/time-of-flight mass spectrometer. Separation occurred over a column - Ascentis C 18 100 × 2.1 mm i.d.; 3.0 μm part size, Supelco, USA) at 40°C. Elution rate was 0.25 mL/min. The elution gradient was as follows: Acetonitrile-water (1:9, v/v) 5 min, acetonitrile-water (1:1, v/v) 15 min, acetonitrile 15 min. The range of detection was m/z 200-800 (atmospheric pressure chemical ionization [APCI], positive ion detection). The potential in the ion source was - 4.5 kV. The drying gas (N 2 ) pressure was 25 kPa. The nebulizer gas (N 2 ) flow rate was 2 L/min. The interface temperature was 350°C. Phytoecdysteroids were identified using data of ultraviolet (UV) detection and mass-spectral data as well as standard retention times. Quantification was carried out on the basis of standard calibration curves using LC Solution version 1.24 (Shimadzu, Kyoto, Japan).

   Results and Discussion Top

The Caryophyllaceae is a large family, with 86 genera and some 2200 species mostly distributed in the Northern Hemisphere in extra-tropical regions. [14]

Until date, approximately 323 species of 66 genera have been analyzed. No positive species have been detected in the genera: Arenaria, Cerastium, Gypsophila, Minuartia, Spergula, Spergularia, and Stellaria. Many positive species occur in other genera: Lychnis, Petrocoptis and Silene. Most data regarding ecdysteroid distribution are available for the Silene/Lychnis complex, into which Melandrium has been subsumed. Among 700 species of Silene of the world flora, 160 has been analyzed and include 96 species containing ecdysteroids, 52 species lacking them and there are controversial data for 12 species. The genus Lychnis numbers about 89 species in the world flora, 24 species of those have been tested for the presence of ecdysteroids, of which 18 are positive, 5 are negative and 1 is uncertain. [15]

2, 3 and their 2-deoxy-derivatives are the most frequently present in the Caryophyllaceae, [3],[16] 2 is usually a predominant component, and the other phytoecdysteroids are in minor amounts.

The experimental data on ecdysteroid distribution in the plant world will possibly bring scholars closer to solving an important ecological problem - clarifying the functions of ecdysteroids in plants as well as allowing us to reveal possible uses of this group of compounds in plant chemotaxonomy.

In this investigation, we have carried out screening of the East Asian representatives of the Caryophyllaceae for 1, 2, 3, and 4 contents [Figure 1].
Figure 1: Chemical structures of ecdysteroids 1-4

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We have improved the described recently method of simultaneous identification of these four ecdysteroids [17] that belong to the same metabolic branch. [18]

Standards of each compound, as well as their mixture, were studied by HPLC with UV sequence and mass-selective detection. We improved conditions for HPLC analysis of the mixture of the four compounds and found that reliable information on ecdysteroid content can be obtained in a short time [13 min, [Figure 2].
Figure 2: High-perfomance liquid chromatography profile of ecdysteroid standard mixture (a); detection: UV 246 nm. Integristerone A (1), 20-hydroxyecdysone (2), ecdysone (3) and 2-deoxy-20-hydroxyecdysone (4) and extract from the aerial part Lychnis fulgens (b)

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While applying standards of the individual ecdysteroids, their elution sequence from nonpolar sorbents was determined as 1 → 2 → 3 → 4 [Figure 2]a. The last two compounds are isomers in their hydroxyl group location, which leads to their good resolvability in the chromatogram. The structure differences of the investigated ecdysteroids [Figure 1] result in some similarities and differences in their mass-spectral patterns. The intensity of the quasi-molecular ions of 2 and 4 comprised 74 and 100%, respectively, and their fragmentation was similar. Contrary to this finding, in the mass spectra of 1 and 3, the intensity of the quasi-molecular ions was 4.5 and 10%, respectively. This can be explained by the instability of the polyhydroxylated intermediates produced by APCI, with a rapid loss of water. [19],[20]

Mass-spectral pattern of 1-4 coincided with data described recently. [21],[17] The using a high-resolution mass-spectrometry allowed to determine the composition of all fragment ions of each investigated components [Table 1].
Table 1: Chromatographic (HPLC) and spectral (UV, MS) characteristics of ecdysteroids 1 - 4

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For extensive screening, it was necessary to apply a sensitive and specific method. We have been employed HPLC for study on the presence or absence of phytoecdysteriods in 64 species (21 genera), which are allocated to 3 subfamilies: Paronychioideae, Alsinoideae and Caryophylloideae. The results of the research on the East Asian ecdysteroids positive Caryophyllaceae are summarized in [Table 2].
Table 2: Contents of integristerone A (1), 20-hydroxyecdysone (2), ecdysone (3) and 2-deoxy-20-hydroxyecdysone (4) in the Caryophyllaceae aerial parts

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Spergularia rubra (L.) J. et C. Presl., (the subfamily Paronychioideae, the tribe Sperguleae Vierh.) has turned out to be ecdysteroid-negative.

In the subfamily Alsinoideae Vierh. no ecdysteroids have been detected in Scleranthus annuus L. (the tribe Sclerantheae Vierh.) and in representatives of the tribe Alsineae Pax: Arenaria redowskii Cham. et Schlecht., Cerastium holosteoides Fries, Cerastium pauciflorum Stev. ex Ser., Cerastium fischerianum Ser., Cerastium beeringianum Cham. et Schlecht., Cerastium arvense L., Eremogone juncea (Bieb.) Fenzl, Eremogone capillaris (Poir.) Fenzl, Eremogone tschuktschorum (Regel) Ikonn., Fimbripetalum radians (L.) Ikonn., Honckenya oblongifolia Torr. et Gray, Minuartia arctica (Stev. ex Ser.) Graebn., Minuartia macrocarpa (Pursh) Ostenf., Minuartia biflora (L.) Schinz et Thell., Minuartia verna (L.) Hiern, Minuartia stricta (Sw.) Hiern, Minuartia sibirica (Regel et Til.) N.S. Pavlova, Moehringia lateriflora (L.) Fenzl, Pseudostellaria sylvatica (Maxim.) Pax, Pseudostellaria rigida (Kom.) Pax, Stellaria bungeana Fenzl, Stellaria graminea L., Stellaria media (L.) Vill., Stellaria eschscholtziana Fenzl, Stellaria fischeriana Ser., Stellaria ruscifolia Pall. ex Schlecht., Stellaria discolor Turcz., Stellaria humifusa Rottb., Stellaria cherleriae (Fisch. ex Ser.) F. Williams, Stellaria longifolia Muehl. ex Willd., Stellaria uliginosa Murr., Stellaria calycantha (Ledeb.) Bong., Stellaria filicaulis Makino and Stellaria dichotoma L.

In the subfamily Caryophylloideae, ecdysteroids have not been revealed in the species of the tribe Diantheae Pax: Dianthus chinensis L., Dianthus repens Willd., Dianthus barbatus L., Dianthus superbus L., Gypsophila pacifica Kom., Gypsophila violacea (Ledeb.) Fenzl, Gypsophila patrinii Ser., Gypsophila davurica Turcz. ex Fenzl, Psammophiliella muralis (L.) Ikonn. As well as in the species of the tribe Lychnideae A. Br.: Oberna behen (L.) Ikonn., Saponaria officinalis L., Melandrium album (Mill.) Garcke, Melandrium olgae Maxim., Melandrium apricum (Turcz. ex Fisch. et Mey.) Rohrb., Agrostemma githago L., Lychnis ajanensis (Regel et Til.) Regel and Silene acaulis (L.) Jacq.

Screening the plants growing in the East Asian have confirmed the data on the absence of ecdysteroids in the species of Arenaria, Cerastium, Gypsophila, Honckenia, Minuartia, Scleranthus, Spergularia, Agrostemma published previously by other researchers. [11],[12],[13],[15]

In a number of genera ecdysteroid-negative as well as ecdysteroid-positive species. Ecdysteroids are detected in Dianthus deltoides and Saponaria bellidifolia, [13] but no ecdysteroids have been found in the East Asian representatives of Dianthus and Saponaria, which shows their patchy distribution within the genus.

We have not detected any ecdysteroids in O. behen, which confirms some other researchers' data [11],[12] on the lack of ecdysteroids in this species; nevertheless, ecdysteroids have been revealed in the individuals of this species growing in the European part of the Russian Federation. [22]

Ecdysteroid-containing species have been detected in the subfamilies Alsinoideae and Caryophylloideae. However, among 34 studied species of 9 genera of the tribe Alsineae of the subfamily Alsinoideae, there is only one ecdysteroid-containing representative-Sagina maxima A. Gray. Ecdysteroids 1, 3, and 4 have not been found [Table 2].

Ecdysteroids have been detected in 10 species of the genera Lychnis, Silene and Melandrium of the tribe Lychnideae, the subfamily Caryophylloideae [Table 2].

Lychnis is represented with five species in the Russian Far East. We analyzed all five species of which four species have turned out to be ecdysteroid-containing ones: Lychnis wilfordii (Regel) Maxim., Lychnis cognata Maxim., Lychnis fulgens Fisch. ex Curt. and Lychnis sibirica L. In Lychnis ajanensis (Regel et Til.) Regel ecdysteroids have not been revealed. This species was described as Melandrium biflorum β. ajanense Regel et Til. [23] Later Regel and Tiling raised taxon to the species. [24] V. N. Voroshilov transferred L. ajanensis to Silene genus (Silene ajanensis (Regel et Tiling) Worosh). [25]

In all four species the predominant compound is 2.

It is the 1 st time that 1 has been found in L. cognata and L. fulgens, 3 in L. cognata, 4 in L. fulgens.

The previous data [13],[26] on the presence of 1, 2 in L. wilfordii and 2 in Lychnis cognate have been confirmed.

Earlier 2, 3 and polypodine B were identified in the Far Eastern L. fulgens.[27] The results of our research have also detected 2 and 3 in this taxon.

The genus Silene is represented with nine species in the Russian Far East. We have investigated five species, of which 4 have turned out to be ecdysteroid-containing: Silene foliosa, Silene stenophylla, Silene jenisseensis (the section Chloranthae (Rohrb.) Schischk.) and Silene repens (the section Spergulifoliae). In S. acaulis (the section Nanosilene Otth.), ecdysteroids have not been detected, although there is some information on the presence of ecdysteroids in this species, in a number of papers. [12],[13],[28]

It is the 1 st time that 1 has been revealed in S. repens Patrin, S. foliosa Maxim., S. stenophylla Ledeb. and S. jenisseensis Willd., maximum content of which reaches 0.49 μg/mg in the aerial part in S. stenophylla during its blooming period. In the aerial part of S. stenophylla and S. jenisseensis, 3 have been detected for the 1 st time.

The predominant component in all the investigated East Asian species of the genus Silene is 2, its content in the aerial part if the investigated species varies from 0.83 μg/mg in S. repens to 4.7 μg/mg in S. stenophylla.

The genus Melandrium is represented with seven species in the Russian Far East. Five species have been analyzed, of which two species turned out to be ecdysteroid-containing. It is the 1 st time that 2 has been found in Melandrium firmum (Siebold et Zucc.) Rohrb. and M. sachalinense (Fr. Schmidt) Schischk., in the latter 1 has been detected as well.

   Conclusion Top

Ecdysteroid-containing species have been detected in two subfamilies of the Caryophyllaceae: Paronychioideae and Caryophylloideae. Most species containing ecdysteroids are representatives of the tribe Lychnideae of the subfamily Caryophylloideae. In the tribe Diantheae (the subfamily Caryophylloideae), no sources of ecdysteroids have been found. It can be asserted that ecdysteroid-containing taxa are confined to the tribe Lychnideae, however, the distribution of ecdysteroids in the genera of the tribe Lychnideae is patchy. Along with genera containing ecdysteroids there are ecdysteroid-negative taxa.

The analysis of ecdysteroid content in the species of Silene, Lychnis and Melandrium revealed that a genus may include species containing ecdysteroids as well as ones in which they have not been identified. In the genus Silene, ecdysteroids have been revealed in the species, which belong to the sections Chloranthae and Spergulifoliae. The plants of these sections are the ones in which finding of new ecdysteroid sources can be prognosed. Data on the quantity of ecdysteroids are available as for several species of Caryophyllaceae of particular interest. According to our results the ecdysteroid content is 4-5 μg/mg in aerial part of Silene species.

Most perspective sources of ecdysteroid are species of the Silene. Perspective sources of ecdysteroids are species from Silene.

   References Top

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  [Figure 1], [Figure 2]

  [Table 1], [Table 2]

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