CC BY
28
Ukrainian Journal of Ecology
Ukrainian Journal ofEcology, 2020, 10(3), 232-237, doi: 10.15421/2020_1579
ORIGINAL ARTICLE
Levels of phenolic compounds in leaves of Eranthis sibirica, E stellata, and E tanhoensis(Ranunculaceae)
V.A. Kostikova1,2*, A.S. Erst1,2, A.A. Kuznetsov2, I.I. Gureyeva2,3
1 Central Siberian Botanical Garden, SB RAS, 101 Zolotodolinskaya Str., Novosibirsk 630090, Russia 2 Tomsk State University, 36 Lenin Ave., Tomsk 634050, Russia 3 Tomsk Oil and Gas Design and Research Institute, 72 Mira Ave., Tomsk 634027, Russia Corresponding author E-mail: serebryako va va@mail. ru Received: 20.08.2020. Accepted22.09.2020
Levels of phenolic compounds in leaves of plants Eranthis sibirica DC., E. stellata Maxim. and E. tanhoensis Erst were studied. In aqueous ethanol extracts from leaves of these Eranthis L. plants, 24 phenolic compounds were identified by highperformance liquid chromatography. These included chlorogenic, gentisic, caffeic, and salicylic acids, quercetin, kaempferol and hyperoside flavonols, and orientin and vitexin flavones. It was revealed that among the three species, the levels of chlorogenic (0.34-0.96 mg/g), caffeic (0.29-0.32 mg/g), and salicylic (0.25 mg/g) acids are higher in leaves of E. sibirica, whereas kaempferol concentration (0.42 mg/g) is higher in E. tanhoensis leaves. Leaves of E. stellata contain more orientin (1.19-4.99 mg/g) and quercetin (0.12-0.20 mg/g) as compared to the other two species. Vitexin (1.84-3.63 mg/g) was found in leaves of E. sibirica only. Species-specific ratios of levels of major phenolic compounds were identified. The total concentration of phenolcarboxylic acids in E. sibirica leaves exceeds almost 2-fold that of flavonols. On the contrary, in E. stellata and E. tanhoensis leaves, the total concentration of flavonols is higher or almost equal to the concentration of phenolcarboxylic acids. Key words. Eranthis sibirica, Eranthisstellata, Eranthis tanhoensis, flavonoid, phenolcarboxylic acid, high-performance liquid chromatography, HPLC.
Introduction
Phenolic compounds are among the most common representatives of secondary metabolites in plant tissues. They play a vital role in the structural integrity of plants, protection from UV radiation, in reproduction, and internal regulation of the physiology and signaling of plant cells (Zaprometov, 1993, Falcone Ferreyra et al., 2012). Due to their high biological activity, plant polyphenols are successfully used in various industries, as well as in medicine and pharmacology, as substances with antioxidant, neuroregulatory, capillary-strengthening, immunomodulatory, anticancer, and other effects (Weinreb et al., 2008; Kim et al., 2011; Bespalov et al., 2017; Alamgir, 2018). In addition, phenolic compounds are widely employed in chemotaxonomic and phylogenetic studies owing to their widespread occurrence among plants, structural diversity, and chemical stability (Vysochina, 2004; Braunberger et al., 2015). In plants of the family Ranunculaceae Juss., phenolic compounds hold promise as chemotaxonomic markers (Hao, 2018; Erst et al., 2020).
Three species of the genus Eranthis L. grow on the territory of Asian Russia: E. sibirica DC., E. stellata Maxim., and E. tanhoensis Erst (Erst et al., 2020). The three taxa belong to section Shibateranthis (Nakai) Tamura. Its species have white flowers and differ from the typical yellow-flowered section Eranthis L. Eranthis sibirica and E. stellata in the pubescence of peduncles, stalks, and fruitlets, leaf blade shape and colour, and the position of the flower (Tamura, 1995). They have different geographic ranges: E. sibirica is widespread in Eastern and Western Siberia, whereas E. stellata grows in the east of China, in Korea, and in the Far East of Russia (Shipchinskij, 1937). Eranthis tanhoensiswas described recently and is an endemic species; it is morphologically similar to E. sibirica and E. stellata because it has white sepals, tubular two-lipped petals with bilobate or forked lips, apically acute lobes with an abaxial lip, and globular yellow protuberances (nectaries) at the top or in the central part (Erst et al., 2020). Eranthis tanhoensis can be found at 350-2400 m above sea level (a.s.l.), where it grows in fir, Siberian pine, spruce, and birch forests, on riverbanks, near streams (up to 1500 m a.s.l.), and in subalpine meadows (at higher altitudes) (Erst et al., 2020). The set and biological activities of compounds from the underground parts of Eranthis plants are being actively studied. Triterpene glycosides of cycloartan and oleanan series and triterpene saponins have been discovered in tubers of E. cilicica Schott. & Kotschy. These substances exert a cytotoxic effect on human promyelocyte leukaemia (HL-60) cells (Watanabe et al., 2003, 2019). Antioxidant properties of chromones isolated from E. cilicicatubers were revealed (Kuroda et al., 2009). Chromones and lectins with anticancer, insecticidal, antifungal, and antiviral effects have been found in tubers of E. hyemalis(L.) Salisb. (Junior, 1979; Kopp et al., 1991; Kumar et al., 1993; George et al., 2011; McConnell et al., 2015; Djafari et al., 2018). The ethanol extract from the roots of E. hyemalishas anti-inflammatory effects (Malik et al., 2017). The whole Eranthisplant is used to treat diuresis and urolithiasis (Hao, 2018). Data on the profile and levels of phenolic compounds in plants of the genus Eranthis are still scarce. We previously revealed the uniqueness of phenolic compounds profile in leaves of Eranthis plants, section Shibateranthis (Erst et al., 2020).
233 Levels of phenolic compounds
The present study aimed to evaluate the levels of phenolic compounds identified by high-performance liquid chromatography (HPLC) in leaves of E sibirica, E. stellata, and E. tanhoensis.
Materials and methods
Leaves of E. sibirica, E. stellata, and E. tanhoensis from natural populations were analyzed for phenolic compounds (Table 1). The material was collected in Irkutsk Oblast, Republic of Buryatia and Primorsky Krai during fruiting in May 2019. The phenolic compounds were studied in 70% aqueous ethanol extracts of leaves; these extracts were prepared by water bath extraction. A certain portion (0.200 g) of the crushed air-dried material was extracted twice: first, with 30 ml for 30 min, then with 20 ml for 20 min. After filtration, the residue in the flask and on the filter was washed with 5 ml of 70% ethyl alcohol. The mixed extract was then concentrated in porcelain cups to 10-15 ml (exact volume). The analysis was performed in duplicate (two biological replicates) (Vysochina, 2004).
An aqueous ethanol extract in the amount of 1 ml was diluted with double-distilled water to 5 ml and passed through a Diapak C16 concentrating cartridge (ZAO BioKhimMak). Substances were washed off the cartridge with a small amount (3 ml) of 70% ethanol and then with 2 ml of 96% ethanol. The mixed eluate was passed through a membrane filter with a pore diameter of 0.45 |jm.
Phenolic compounds in the eluate were investigated on an analytical HPLC system that consisted of an Agilent 1200 liquid chromatograph (USA) (column: Zorbax SB-C18, 4.6 x 150 mm, 5 pm) equipped with a diode array detector, an autosampler, and a ChemStation system for collecting and processing chromatographic data by the method of T.A. van Beek (2002), with modifications. The separation was carried out under the following conditions: a gradient from 31 % to 33% methanol acidified with orthophosphoric acid (0.1%) for 27 min, then the methanol level in the mobile phase in the aqueous solution of orthophosphoric acid (0.1 %) was raised from 33% to 46% within 11 min; next, it was changed from 46% to 56% over the next 12 min and from 56% to 100% within 4 min. The flow rate of the eluent was 1 ml/min, column temperature 26 °C, and injected-sample volume was 10 pl. Detection was performed at A = 255, 270, 290, 340, 360, and 370 nm.
Quantitative determination of individual phenolic compounds in the plant samples was conducted by the external-standard method at A = 255 nm. To prepare the standard samples, we used salicylic and chlorogenic acids, quercetin, kaempferol, orientin (Sigma-Aldrich), gentisic and caffeic acids (Serva), and vitexin (Fluka). The concentration of the standard solutions was 10 pg/ml. Comparative analysis of the levels of individual-group of phenolic compounds in the plant leaf extracts was performed by the integrated intensity of the chromatographic signal of the phenolic compound at A = 360 nm. Quantitative processing of the data was performed in Microsoft Excel.
Table 1. Sites of collection of the studied Eranthisspecimens
Sample^ Locality, date, and collector
number*
E. sibirica
Russia, Irkutsk Oblast, Slyudyansky Distr., Burovshina Riv.; 51 °37'06.00"N, 103°49'16.17''E; alt. 470 m; 02.05.2019. S1 A.S. Erst, D.A. Krivenko, O.A. Chernysheva
Russia, Irkutsk Oblast, Slyudyansky Distr., vicinity of Slyudyanka town; 51°38'02.94''N, 103°41'13.90"E; alt. 531 m; S2 02.05.2019.A.S. Erst, D.A. Krivenko, O.A. Chernysheva
E. stellata
Russia, Primorsky Krai, Vladivostok City, Malaya Sedanka Riv.; 43°12'37.9"N131 °59'39.1 "E; alt. 59 m. 16.05.2018. St3 V.Yu. Nikulin, A.Yu. Nikulin
Russia, Primorsky Krai, Vladivostok city, 13 km St.; 43°11 '32.3"N,131 °55'49.0"E; alt. 103 m; 14.05.2019. V.Yu. Nikulin, A.Yu. Nikulin
Russia, Primorsky Krai, Vladivostok City, Ostrov Russkij; 42°59'05.0"N, 131 °51 '51.5"E; alt. 74 m; 12.05.2019. V.Yu. Nikulin, A.Yu. Nikulin
E. tanhoensis
T6 Russia, Irkutsk Oblast, Slyudyansky Distr., Malye Mangaly (Kuytun) Riv.; 51 °26'48.17''N, 104°34'16.62''E; alt. 471 m;
02.05.2019.A.S. Erst, D.A. Krivenko, O.A. Chernysheva T7 Russia, Buryatia Republic, Kabansky Distr., Tolbazikha Riv. 51 °26'21.06''N, 104°41 '09.82"E; alt. 471 m; 01.05.2019. _A.S. Erst, D.A. Krivenko, O.A. Chernysheva_
Note. Leaves are taken from 5 - 6 plants.
Results and discussion
In 70% aqueous ethanol extracts from leaves of the three studied plant species of the genus Eranthis, 24 phenolic compounds were found previously (Erst et al., 2020) 24 phenolic compounds were identified here. The identified compounds included chlorogenic, gentisic, caffeic, and salicylic acids, quercetin, kaempferol and hyperoside flavonols, orientin, and vitexin flavones. Hyperoside was found only in the aqueous ethanol leaf extracts of the plants in the flowering phase. The studied species turned out to be very similar in the set of phenolic compounds in leaves; however, they contain phenolic compounds specific for each
taxon in question. It was revealed that E. sibirica and E. tanhoensis are closer in terms of secondary metabolism. Eranthis stellata is well distinguished from the other two species. In contrast to E. tanhoensis, the chromatographic profile of E. sibirica contains caffeic acid, orientin, vitexin, and flavone 6 in the aqueous ethanol leaf extracts. Leaves of E. tanhoensis from almost all the studied populations were found to contain quercetin, which was not detectable in E. sibirica. The compounds identified in E. stellata leaf extracts specifically were gentisic acid, phenolic acid 4, and flavone 21 (i.e., they were not found in the other two species). Vitexin, hyperoside, and salicylic acid were not observed previously in leaves of E. stellata (Erst et al., 2020). Samples from different populations of the same Eranthis species could be distinguished by the presence of minor phenolic compounds in leaf extracts (Table 2). For example, salicylic acid was detectable in leaves of the E. sibirica growing in the Slyudyanka town vicinity (S2). Eranthissibiricafrom another population growing in Burovshina River valley (S1) does not contain salicylic acid. Flavone 20 was identified only in aqueous ethanol leaf extracts of E. sibiricasample S1. Phenolic acid 14 was found in leaves of E. stellata growing in the vicinity of Vladivostok city and in Malaya Sedanka River valley, whereas in St5 plants, this phenolic acid was not observed. Besides, E. stellata specimens from Malaya Sedanka River valley (St3) are distinguished by the presence of flavonol 18 in leaves (Table 2). Leaves of E. tanhoensis specimens from Tolbazikha River valley (T7) contain phenolic acid 14 and kaempferol. E. tanhoensis specimens collected in Malye Mangaly River valley (T6) contain quercetin in their leaves (Table 2). The observed species specificity of the chromatographic profiles of E. sibirica, E. stellata, and E. tanhoensis indicates their species independence, as proved by morphological and molecular data (Wahlsteen, 2016; Park et al., 2019; Erst et al., 2020). At the same time, the similarity of biochemical patterns and different geographic ranges of E. stellata and E. sibiricafavour the opinion of some scientists that these species have developed in parallel from a common ancestor. Several taxa closely related to these species grow in China and Japan (Popov, 1959, Kiseleva, 1978).
Table 2. Description of the phenolic compounds found in leaf extracts of Eranthis species
Peak No. Phenolic compound Retention time (tR), min Spectral characteristic Amax, nm E sibirica Sample number E stellata E tanhoensis
1 Chlorogenic acid 3.2 244, 300 sh., 325 S1, S2 St3, St4, St5 T6, T7
2 Gentisic acid 4.1 240, 330 - St3, St4, St5 -
3 Caffeic acid 5.2 240, 290 sh., 320 S1, S2 St3, St4, St5 -
4 Phenolic acid 4* 7.1 250, 300 - St3, St4, St5 -
5 Orientin 8.9 250, 350 S1, S2 St3, St4, St5 -
6 Flavone 6* 9.4 270, 310 S1, S2 - -
7 Phenolic acid 7 10.0 250, 290 sh., 335 S1, S2 St3, St4, St5 T6, T7
8 Vitexin 12.1 270, 340 S1, S2 - traces
9 Flavonol 9* 15.1 255, 270 sh., 300 S1, S2 St3, St4, St5 T6, T7
10 Hyperoside 18.4 255, 268 sh., 355 during during
flowering flowering
11 Salicylic acid 19.8 240, 305 S2 - T6, T7
12 Phenolic acid 12* 20.9 240, 290 sh., 335 S1, S2 St3, St4, St5 T6, T7
13 Flavonol 13* 22.3 255, 360 - St3, St4, St5 T6, T7
14 Phenolic acid 14* 25.4 255, 300 S1, S2 St3, St4 T7
15 Flavonol 15* 32.7 270, 310, 365 S1, S2 St3, St4, St5 T6, T7
16 Phenolic acid 16* 34.5 250, 290, 330 S1, S2 St3, St4, St5 T6, T7
17 Flavone 17* 36.9 250, 325 S1, S2 St3, St4, St5 T6, T7
18 Flavonol 18* 38.7 255, 305, 360 S1, S2 St3 T6, T7
19 Quercetin 40.1 255, 372 - St3, St4, St5 T6
20 Flavone 20* 41.6 265, 320 S1 - -
21 Flavone 21* 42.2 270, 310 - St3, St4, St5 -
22 Flavanone 22* 43.4 275, 315 S1, S2 - T6, T7
23 Phenolic acid 23* 44.3 255, 300, 330 S1, S2 St3, St4, St5 T6, T7
24 Kaempferol 47.3 266, 370 - St3, St4, St5 T7
Note. * - group of compounds identified by spectral characteristics (Zaprometov, 1993; Klyshev et al., 1978; Zaprometov, 1993); "-" compound was not detected; sh. - shoulder (traces of a signal)
Among the studied Era nth is species, a quantitative comparison of the phenolic compounds we identified in the aqueous ethanol leaf extracts showed that the levels of chlorogenic (0.34-0.96 mg/g), caffeic (0.29-0.32 mg/g), and salicylic acids (0.25 mg/g) are
235 Levels of phenolic compounds
higher in leaves of E. sibirica, and the level of kaempferol (0.42 mg/g) is higher in leaves of E. tanhoensis(Table 3). In aqueous ethanol leaf extracts of E. stellata, concentrations of orientin (1.19-4.99 mg/g) and quercetin (0.12-0.20 mg/g) are higher than those in the other two species; vitexin (1.84-3.63 mg/g) was found in leaves of E. sibirica only (Table 3).
Table 3. Concentrations of phenolic compound in leaves of three Era nth is species (mg/g of air-dried material)
Compound
Chlorogenic acid Gentisic acid Caffeic acid Orientin Vitexin Salicylic acid Quercetin Kaempferol
E. sibirica
Sample number E. stellata
E. tanhoensis
S1
0.96±0.04
0.32±0.01 0.69±0.03 1.84±0.07
S2
0.34±0.01
0.29±0.01 2.94±0.11 3.63±0.13 0.25±0.01
St3 0.19±0.01
0.19±0.01
0.09±0.00
2.50±0.09
St4 0.37±0.01
0.24±0.01
0.32±0.01
4.99±0.18
St5 0.11±0.00
0.02±0.00
0.20±0.01
1.19±0.04
T6 0.34±0.01
T7 0.71 ±0.03
0.20±0.01 0.31±0.01
0.12±0.00 0.15±0.01
0.17±0.01 0.20±0.01
0.18±0.01 0.07±0.00
0.19±0.01
0.42±0.02
Note. The data presented like means and standard errors (n = 3).
The main phenolic compounds in the plant extracts under study are phenolic acid 7, phenolic acid 12, and flavonol 9. Analysis of concentration ratios of the main phenolic compounds uncovered significant differences among studied Eranthis species (Fig. 1). In leaves of E. sibirica, the level of phenolic acid 12 in sample S1 and phenolic acid 7 in sample S2 exceeds that of flavonol 9. Flavonol 9 is dominant in leaf extracts of E. stellata and E. tanhoensis (Fig. 1). The flavonol 9-to-phenolic acid 12 ratio in E. sibirica sample S1 is 0.69; in sample S2, it amounts to 0.72; and among E. stellata samples, it varies from 1.49 to 1.85. In E. tanhoensis, the ratio of the main phenolic compounds is much higher than that in the other two species: 5.48 in sample T6 and 5.66 in sample T7. This ratio may be a species marker for the studied Eranthis species. Nonetheless, the ratio should be verified on a larger number of samples.
Fig. 1. A comparison of concentrations of the main phenolic compounds in aqueous ethanol extracts of Eranthis sibirica (samples S1 and S2), E. stellata (St3, St4, and St5), and E. tanhoensis (T6 and T7). The X-axis is the sample number; the Y-axis indicates the integrated intensity of a chromatographic signal of a phenolic compound, %.
The three analyzed Eranthis species differ in the concentration ratio of total phenolcarboxylic acids to total flavonols in leaves (Fig. 2). In leaves of E. sibirica, the total concentration of phenolcarboxylic acids exceeds almost 2-fold that of flavonols (Fig. 2). On the contrary, the total level of flavonols in leaves of E. stellata and E. tanhoensis is higher or almost equal to that of phenolic acids (Fig. 2). It is important to note that the total level of flavones in these plant leaves is less than that of phenolcarboxylic acids and flavonols. The only exception is E. sibirica sample S2 collected in the vicinity of Slyudyanka town because its leaves contain more flavones than flavonols (Fig. 2).
- _ Phenolcarboxylic
acids
- □ - Flavonols
□ - Flavones
SI S2 St3 St4 Sti T6 T7
Fig. 2. A comparison of levels of phenolic-compound classes in leaves of Eranthis sibirica (samples S1 and S2), E. stellata (St3, St4, and St5), and E tanhoensis(T6 and T7). The X-axis is the sample number; the Y-axis indicates the integrated intensity of a chromatographic signal of a phenolic compound, %.
These differences in the levels of phenolic compounds may be due to dissimilarity of growth conditions of the plants in question. Phenolic compounds play a crucial role in plant adaptation to unfavourable environmental conditions and increase ecological plasticity of plants. These compounds also protect against UV radiation and other stress factors (Zaprometov, 1993, Vysochina, 2004, Karakulov et al., 2018). Eranthis sibirica grows in the continental climate of the mountainous terrain in Irkutsk Oblast. Specimens of E sibiricawere collected at an altitude of 470-531 m a.s.l. Probably, these conditions promote the accumulation of phenolcarboxylic acids in leaves. E. stellata grows under milder conditions of the moderate monsoon climate in Primorsky Krai, and the plant specimens were collected at a relatively low altitude of 59-103 m a.s.l. The increased level of insolation in Primorsky Krai may facilitate the accumulation of flavonols in E stellata leaves. Nevertheless, the concentration ratio of total phenol carboxylic acids to total flavonols in the leaves of E tanhoensis, which like E sibirica grows in the continental climate of the mountainous terrain in Irkutsk Oblast, indicates species specificity of the levels of phenolic compounds, as demonstrated in other plant species (Khramova & Andysheva, 2014, Raal et al., 2015). In leaves of E tanhoensis, the level of flavonols is higher or almost equal to that of phenolcarboxylic acids, thus showing its similarity to E stellata growing in Primorsky Krai in terms of the levels of these substances.
Conclusion
Phenolic compounds identified in aqueous ethanol leaf extracts by HPLC are quantitated for the first time in plants of the genus Eranthis, namely, white-flowered species of the section Shibateranthis. E. sibirica, E. stellata, and E tanhoensis. Among the three species, concentrations of chlorogenic (0.34-0.96 mg/g), caffeic (0.29-0.32 mg/g), and salicylic acids (0.25 mg/g) were found to be higher in E sibirica leaves, and the highest concentration of kaempferol (0.42 mg/g) was observed in leaves of E tanhoensis. Eranthis stellata leaves contain more orientin (1.19-4.99 mg/g) and quercetin (0.12-0.20 mg/g) as compared to the other two species. Vitexin (1.84-3.63 mg/g) was detectable in leaves of E sibirica only. A species-specific ratio of levels of the main phenolic compounds in leaves was identified in the three studied species of the genus Eranthis. The total concentration of phenolcarboxylic acids in E sibirica leaves exceeds almost 2-fold that of flavonols. On the contrary, the total concentration of flavonols in E stellata and E tanhoensis leaves is higher or almost equal to that of phenolcarboxylic acids. In terms of the chromatographic profile, E tanhoensis is closer to E sibirica, and in terms of phenolic compounds levels, to E stellata.
Acknowledgements
We would like to express our gratitude to V.Yu. Nikulin and A.Yu. Nikulin from the Federal Scientific Center of East Asian Terrestrial Biodiversity, the Far Eastern Branch of the Russian Academy of Sciences, for sample collection in Primorsky Krai and to D.A. Krivenko and O.A. Chernysheva from the Siberian Institute of Plant Physiology and Biochemistry, the Siberian Branch of the Russian Academy of Sciences, for assistance with sample collection in Irkutsk Oblast.
The work was supported by the Russian Foundation for Basic Research, grant No 18-34-20056 mol_a_ved, by the Tomsk State University competitiveness improvement programme under grant No 8.1.27.2020 and with financial support from the grant of the President of the Russian Federation for the state support of young Russian scientists and candidates of Sciences (project No MK-1045.2020.4).
References
Alamgir, A. N. M. (2018). Therapeutic Use of Medicinal Plants and Their Extracts. 2. Phytochemistry And Bioactive Compounds. Switzerland, 849 p.
237 Levels of phenolic compounds
Bespalov, V.G., Alexandrov, V.A., Vysochina, G.I, Kostikova, V.A., Semenov, A.L. & Baranenko, D. (2018). Inhibitory Effect of Filipendula ulmariaon Mammary Carcinogenesis Induced by Local Administration of Methylnitrosourea to Target Organ in Rats. Anti-cancer agents in medicinal chemistry, 18 (8), 1177-1183. https://doi.org/10.2174/1871520618666180402125913. Braunberger, C., Zehl, M., Conrad, J., Wawrosch, C., Strohbach, J., Beifuss, U. & Krenn, L. (2015). Flavonoids as chemotaxonomic
markers in the genus Drosera. Phytochemistry, 118, 74-82. https://doi.org/10.1016Z.phytochem.2015.08.017 Djafari, J., McConnell, M. T., Santos, H. M., Capelo, J. L., Bertolo, E., Harvey, S. C., Lodeiro, C. & Fernandez-Lodeiro, J. (2018). Synthesis of Gold Functionalised Nanoparticles with the Eranthis hyemalis Lectin and Preliminary Toxicological Studies on Caenorhabditis elegans. Materials (Basel), 11 (8), 1363. https://doi.org/10.3390/ma11081363. Erst, A.S., Sukhorukov, A.P., Mitrenina, E.Y., Skaptsov, M.V., Kostikova, V.A., Chernisheva, O.A., Troshkina, V., Kushunina, M., Krivenko, D.A., Ikeda, H. & Xiang, K. (2020). An integrative taxonomic approach reveals a new species of Eranthis (Ranunculaceae) in North Asia. PhytoKeys, 140, 75-100. Falcone Ferreyra, M.L., Rius, S. & Casati, P. (2012). Flavonoids: Biosynthesis, Biological Functions and Biotechnological
Applications. Frontiers in plant science, 3, 1 -15. George, O., Solscheid, C., Bertolo, E. & Lisgarten, D. (2011). Extraction and purification of the lectin found in the tubers of Eranthis
hyemalis (winter aconite). Journal of Integrated OMICS, 1(2), 268-272. https://doi.org/10.5584/jiomics.v1i2.72. Hao, D. C. (2018). Ranunculales Medicinal Plants: Biodiversity, Chemodiversity and Pharmacotherapy. New York, 393 p. Junior, P. (1979). Eranthin and eranthin-b-D-glucoside: two new chromones from Eranthishiemalis. Phytochemistry, 18, 20532054.
Karakulov, A. V., Karpova, E. A. & Vasiliev, V. G. (2018). Ecological and geographical variation of morphometric parameters and
flavonoid composition of Rhododendronparvifolium. Turczaninowia, 21, 2, 133-144. (In Russian). Khramova, E.P. & Andysheva, E.V. (2014). Phenolic compounds of Pentaphylloides species (Rosaceae) from the Russian Far East.
Rastitel'nyj mir Aziatskoj Rossii, 2 (14), 65-70. (In Russian). Kim, W., Seong, K. M. & Youn, B. (2011). Phenylpropanoids in Radioregulation: Double Edged Sword. Exp. Mol. Med, 43 (6), 323333.
Kiseleva, A. A. (1978). Nemoral relics in the flora of the southern coast of the Lake Baikal. Bot. zhurn., 65 (11), 1647-1656. (In Russian).
Klyshev, L. K., Bandyukova, V. A. & Alyukina, L. S. (1978). Flavonoidy rasteniy [Plant flavonoids]. Alma-Ata: Nauka, 220. (In Russian).
Kopp, B., Kubelka, E., Reich, C., Robien, W. & Kubelka, W. (1991). 4H-Chromenone glycosides from Eranthis hyemalis (L.)
Salisbury. Helv. Chim. Acta, 74, 611 -616. Kumar, M. A., Timm, D., Neet, K., Owen, W., Peumans, W. J. & Rao, A. G. (1993). Characterization of the lectin from the bulbs of Eranthis hyemalis (winter aconite) as an inhibitor of protein synthesis. Journal of Biological Chemistry, 268, 25176-25183. Kuroda, M., Uchida, S., Watanabe, K. & Mimaki, Y. (2009). Chromones from the tubers of Eranthis cilicica and their antioxidant
activity. Phytochemistry, 70, 288-293. https://doi.org/10.1016/j.phytochem.2008.12.002 Malik, J., Tauchen, J., Landa, P., Kutil, Z., Marsik, P., Kloucek, P., Havlik, J. & Kokoska, L. (2017). In vitro antiinflammatory and antioxidant potential of root extracts from Ranunculaceae species South African. Journal of Botany, 109, 128-137. https://doi.org/10.1016/j.sajb.2016.12.008 McConnell, M.-T., Lisgarten, D. R., Byrne, L. J., Harvey, S. C. & Bertolo, E. (2015). Winter Aconite (Eranthis hyemaiis) Lectin as a
cytotoxic effector in the lifecycle of Caenorhabditis elegans. PeerJ. 3: e1206. https://doi.org/oi:10.7717/peerj.1206. Park, S. Y., Jeon, M. J., Ma, S. H., Wahlsteen, E., Amundsen, K., Kim, J. H., Suh, J. K., Chang, J. S. & Joung, Y. H. (2019). Phylogeny and genetic variation in the genus Eranthis using nrITS and cpIS single nucleotide polymorphisms. Horticulture, Environment and Biotechnology, 60, 239-252. https://doi.org/10.1007/s13580-018-0113-0 Popov, M. G. (1959). Flora Srednej Sibiri [Flora of Central Siberia]. Moscow; Leningrad: AS USSR Publ., 2, 559-917. (In Russian). Raal, A., Boikova, T. & Püssa, T. (2015). Content and Dynamics of Polyphenols in Betulaspp. Leaves Naturally Growing in Estonia. Rec. Nat. Prod., 9 (1), 41-48.
Shipchinskij, N.V. (1937). Vesennik - EranthisSalisb. In: Flora SSSR [Flora of the USSR], 7. Moscow-Leningrad. AS USSR Publ., 6062. (In Russian).
Tamura, M (1995) Eranthis. In: Hiepko P (Ed.). Die Natürlichen Pflanzenfamilien, 17(4). Duncker und Humblot, Berlin, 253-255. Van Beek, T. A. (2002). Chemical analysis of Ginkgo biloba leaves and extracts. J. Chromatogr A, 967, 21 -35. Vysochina, G. I. (2004). Fenolnye soyedineniya v sistematike i filogenii semeistva grechishnykh. Novosibirsk, 240 p. (In Russian). Watanabe, K., Mimaki, Y., Fukaya, H. & Matsuo, Y. (2019). Cycloartane and Oleanane Glycosides from the Tubers of Eranthis
cilicica. Molecules, 24 (1), 69-81. https://doi.org/10.3390/molecules24010069. Watanabe, K., Mimaki, Y., Sakuma, C. & Sashida, Y. (2003). Eranthisaponins A and B, two new bisdesmosidic triterpene saponins
from the tubers of Eranthis cilicica. J. Nat. Prod., 66, 879-882. https://doi.org/10.1021 /np030071 m Weinreb, O., Amit, T. & Youdim, M. (2008). The Application of Proteomics for Studying the Neurorescue Activity of the Polyphenol
(-)-epigallocatechin-3-gallate. Arch. Biochem. Biophys, 476 (2), 152-160. Zaprometov, M. N. (1993). Fenolnye Soedineniya: rasprostranenie, metabolizm i funkcii v rasteniyah [Phenolic Compounds:
Distribution, Metabolism, and Function in Plants]. Moscow, 271 p. (In Russian). Citation:
Kostikova, V.A., Erst, A.S., Kuznetsov, A.A., Gureyeva, I.I. (2020). Levels of phenolic compounds In leaves of Eranthissibirica, E. stellata, and £ tanhoensis (Ranunculaceae). Ukrainian Journal of Ecology, 10(3), 232-237. | (c<0This work Is licensed under a Creative Commons Attribution 4.0. License
