Total phenolic compounds and antioxidant capacity of six species of Actaea L. (Ranunculaceae)

Abstract

Six species of the genus Actaea (Ranunculaceae) were analyzed for contents of soluble phenolic compounds, including flavonols, catechins, phenolic acids, coumarins, and tannins. Additionally, the contents of saponins, carotenoids, and chlorophylls a and b were determined. Extracts from the aboveground and underground parts of the studied plant species were tested for antioxidant activity using the DPPH assay. Based on the total phenolic content, four categories could be distinguished, regardless of species: “stems” (up to 22.7 mg/g), “roots” (up to 33.3 mg/g), “leaves” (up to 50.6 mg/g), and “inflorescences” (59.9 mg/g). An exception was the leaf extract of Actaea erythrocarpa, which had the highest concentration of phenolic compounds among all the plant samples, at 60.6 mg/g. The analysis of antioxidant activity revealed the same categories: the highest antiradical activity was shown by extracts from the leaves and inflorescences of A. erythrocarpa and A. cimicifuga. Thus, our assays indicate that extracts from the leaves and inflorescences of A. erythrocarpa and A. cimicifuga contain high concentrations of phenolic compounds, which correlate with their antiradical activity.

Keywords

• Actaea sp.
• Antioxidant activity
• Actaea asiatica
• Actaea rubra
• Actaea podocarpa

References

1. Amorim, E., Castro, V., Melo, J., CorreÌa, A., & Peixoto Sobrinho, T.J. (2012). Standard operating procedures (SOP) for the spectrophotometric determination of phenolic compounds contained in plant samples. In: Akyar I (Ed) Latest Research into Quality Control. Rijeka: Croatia InTech, pp 47–66.
2. Bittner, M., Schenk, R., Springer, A., Melzig, M.F. (2016). Economical, plain, and rapid authentication of Actaea racemosa L. (syn. Cimicifuga racemosa, Black Cohosh) herbal raw material by resilient RP-PDA-HPLC and chemometric analysis. Phytochemical Analysis, 27, 318–325. https://doi.org/10.1002/pca.2622
3. Borrelli, F., & Ernst, E. (2002). Cimicifuga racemosa: a systematic review of its clinical efficacy. European Journal of Clinical Pharmacology, 58, 235–241. https://doi.org/10.1007/s00228-002-0457-2
4. Brighente, I.M.C., Dias, M., Verdi, L.G., & Pizzolatti, M.G. (2007). Antioxidant activity and total phenolic content of some Brazilian species. Pharmaceutical Biology, 45, 156–161. https://doi.org/10.1080/13880200601113131
5. Burdette, J.E., Chen, S.N., Lu, Z.Z., Xu, H.Y., White, B.E.P., Fabricant, D.S., Liu, J.H., Fong, H.H.S., Farnsworth, N.R., Constantinou, A.I., Breemen, R.B.V., Pezzuto, J.M., & Bolton, J.L. (2002). Black cohosh (Cimicifuga racemosa L.) protects against menadione-induced DNA damage through scavenging of reactive oxygen species: bioassay-directed isolation and characterization of reactive oxygen species: bioassay-directed isolation and characterization of active principles. Journal Agricultural and Food Chemistry, 50(24), 7022–7028. https://doi.org/10.1021/jf020725h
6. Chinese Pharmacopoeia Commission (2015). The pharmacopoeia of Chinese People`s Republic. China medical science press, Beijing, pp. 73–74.
7. Compton, J., Culham, A., Gibbings, J., & Jury, S. (1998a). Phylogeny of Actaea including Cimicifuga (Ranunculaceae) inferred from nrDNA ITS sequence variation. Biochemical Systematics and Ecology, 26, 185–197. https://doi.org/10.1016/S0305-1978(97)00102-6
8. Compton, J.A., Culham, A., & Jury, S.L. (1998b). Reclassification of Actaea to include Cimicifuga and Souliea (Ranunculaceae): Phylogeny inferred from morphology, nrDNA ITS, and cpDNA trnL-F sequence variation. Taxon, 47(3), 593–634. https://doi.org/10.2307/1223580

9. Da, Y., Niu, K., Wang, K., Cui, G., Wang, W., Jin, B., Sun, Y., Jia, J., Qin, L., & Bai, W. (2015). A comparison of the effects of estrogen and Cimicifuga racemosa on the lacrimal gland and submandibular gland in ovariectomized rats. PLoS ONE, 10, e012147. https://doi.org/10.1371/journal.pone.0121470.
10. Disch, L., Forsch, K., Siewert, B., Drewe, J., & Fricker, G. (2017). In vitro and in situ characterization of triterpene glycosides from Cimicifuga racemosa extract. Journal of Pharmaceutical Sciences, 106, 3642–3650. https://doi.org/10.1016/j.xphs.2017.07.023
11. Djeridane, A., Yousfi, M., Nadjemi, B., Boutassouna, D., Stocker, P., & Vidal, N. (2006). Antioxidant activity of some Algerian medicinal plants extracts containing phenolic compounds. Food Chemistry, 97(4), 654–660. https://doi.org/10.1016/j.foodchem.2005.04.028
12. Ermakov, A.I., Arasimovich, V.V., Yarosh, N.P., Peruanskiy, Y.V., Lukovnikova, G.A., & Ikonnikova, M.I. (1987). Методы биохимического исследования растений [Methods of Biochemical Investigation of Plants]; Agropromizdat: Leningrad, Russia.
13. Erst, A.S., Sukhorukov, A.P., Mitrenina, E.Y,, Skaptsov, M.V., Kostikova, V.A., Chernisheva, O.A., Troshkina, V., Kushunin,a M., Krivenko, D.A., Ikeda, H., Xiang, K., & Wang, W. (2020). An integrative taxonomic approach reveals a new species of Eranthis (Ranunculaceae) in North Asia. PhytoKeys, 140, 75-100. https://doi.org/10.3897/phytokeys.140.49048
14. Erst, A.S., Petrova, N.V., Kaidash, O.A., Wang, W., & Kostikova, V.A. (2023). The Genus Eranthis: Prospects of Research on Its Phytochemistry, Pharmacology, and Biotechnology. Plants, 12, 3795. https://doi.org/ 10.3390/plants12223795
15. Fedoseeva, L.M. (2005). Изучение дубильных веществ подземных и надземных вегетативных органов бадана толстолистного (Bergenia crassifolia (L.) Fitsch.), произрастающего на Алтае [The study of tannins of underground and aboveground vegetative organs of the Bergenia crassifolia (L.) Fitsch., growing in Altai]. Chemistry of Plant Raw Materials, 2, 45–50.
16. Foster, S. (1999). Black cohosh: Cimicifuga racemosa. A literature review. HerbalGram, 45, 35–50.
17. Gawron-Gzella, A., Witkowska-Banaszczak, E., Bylka, W., Dudek-Makuch, M., Odwrot, A., & Skrodzka, N. (2016). Chemical composition, antioxidant and antimicrobial activities of Sanguisorba officinalis L. extracts. Pharmaceutical Chemistry Journal, 50, 244–249. https://doi.org/10.1007/s11094-016-1431-0
18. Hashida, M. (2011). Cimicifuga rhizome. The Japanese pharmacopoeia, sixteenth ed. Ministry of Health, Labour and Welfare, Tokyo, pp. 1622–1623.
19. He, K., Pauli, G.F., Zheng, B.L., Wang, H.K., Bai, N.S., Peng, T.S., Roller, M., & Zheng, Q.Y. (2006). Cimicifuga species identification by high performance liquid chromatography-photodiode array/mass pectrometric/evaporative light scattering detection for quality control of black cohosh products. Journal of Chromatography A, 1112, 241–254. https://doi.org/10.1016/j.chroma.2006.01.004.
20. Jiang, B., Yang, H., Nuntanakorn, P., Balick, M.J., Kronenberg, F., & Kennelly, E.J. (2005). The value of plant collections in ethnopharmacology: A case study of an 85-year-old black cohosh (Actaea racemosa L.) sample. Journal of Ethnopharmacology, 96, 521–528. https://doi.org/10.1016/j.jep.2004.09.049.
21. Kalendar O.V., Kostikova V.A., Kukushkina T.A., Erst A.S., Kuznetsov A.A., Kulikovskiy M.S., & Vasilyeva O.Y. (2023). Seasonal development of Paeonia obovata and Paeonia oreogeton and their contents of biologically active and reserve substances in the forest-steppe zone оf Western Siberia. Horticulturae, 9, 102. https://doi.org/10.3390/horticulturae9010102
22. Katanić, J., Boroja, T., Stanković, N., Mihailović, V., Mladenović, M., Kreft, S., & Vrvić, M.M. (2015). Bioactivity, stability and phenolic characterization of Filipendula ulmaria (L.) Maxim. Food Funct, 6, 1164–1175. https://doi.org/10.1039/c4fo01208a.
23. Kostikova, V.A., Petrova, N.V., Chernonosov, A.A., Koval, V.V., Kovaleva, E.R., Wang, W., & Erst, A.S. (2024). Chemical composition of methanol extracts from leaves and flowers of Anemonopsis macrophylla (Ranunculaceae). International Jounal of Molecular Sciences, 25, 989. https://doi.org/10.3390/ ijms25020989
24. Kukushkina, T.A., Kostikova, V.A., & Khramova, E.P. (2024). Содержание катехинов в листьях и корнях Сomarum salesovianum и Сomarum palustre (Rosaceae) [Сontent of catechins in leaves and roots of Сomarum salesovianum and Сomarum palustre (Rosaceae)]. Chemistry of Plant Raw Materials, 2, 196–206. https://doi.org/10.14258/jcprm20240212561
25. Kumarasamy, Y., Byres, M., Cox, P.J., Jaspars, M., Nahar, L., & Sarker, S.D. (2007). Screening seeds of some Scottish plants for free radical scavenging activity. Phytotherapy Research, 21, 615–621. https://doi.org/10.1002/ptr.2129
26. Li, X.C., Lin, J., Gao, Y.X., Han, W.J., & Chen, D.F. (2012). Antioxidant activity and mechanism of Rhizoma Cimicifugae. Chemistry Central Journal, 6(1), 140–149. https://doi.org/10.1186/1752-153X-6-140
27. Ling, Y.Y., Xiang, K.L., Peng, H.W., Erst, A.S., Lian, L., Zhao, L., Jabbour, F., & Wang, W. (2023). Biogeographic diversification of Actaea (Ranunculaceae): Insights into the historical assembly of deciduous broad-leaved forests in the Northern Hemisphere. Molecular Phylogenetics and Evolution, 186, 107870. https://doi.org/10.1016/j.ympev.2023.107870.
28. Luferov, A.N. (2004). Таксономический конспект лютиковых (Ranunculaceae) Дальнего Востока России [A taxonomic synopsis of Ranunculaceae of the Far East of Russia]. Turczaninowia, 7(1), 1–85.
29. Luo, J.P., Wang, L., Ren, C., Yang, Q.E., & Yuan, Q. (2016). Taxonomic notes on Cimicifuga nanchuanensis (Ranunculaceae), a hitherto imperfectly known species from China. Nordic Journal of Botany, 34, 87–101. https://doi.org/10.1111/njb.00937
30. Mao, J.L. (1996). Functional tea for health care. Beijing science and technology press, Beijing.
31. Nuntanakorn, P., Jiang, B., Yang, H., Cervantes-Cervantes, M., Kronenberg, F., & Kennelly, E.J. (2007). Analysis of polyphenolic compounds and radical scavenging activity of four American Actaea species. Phytochemical Analysis, 18, 219–228. https://doi.org/10.1002/pca.975
32. Pisarev, D.I., Martynova, N.A., Netrebenko, N.N., Novikov, O.O., & Sorokopudov, V.N. (2009). Сапонины и их определение в корневищах аралии манчжурской в условиях Белгородской области [Saponins and their determination in the rhizomes of aralia manchurian from the Belgorod region]. Khimija rastitel'nogo syr'ja, 4, 197–198.
33. Rashid, S., Rashid, K., Ganie, A.H., Nawchoo, I.A., Tantry, M.A., & Khuroo, A.A. (2023). A review of the genus Actaea L.: ethnomedical uses, phytochemical and pharmacological properties. Journal of Herbal Medicine, 41, 100690. https://doi.org/10.1016/j.hermed.2023.100690
34. Sakakibara. H., Honda, Y., Nakagawa, S., Ashida, H., & Kanazawa, K. (2003). Simultaneous determination of all polyphenols in vegetables, fruits, and teas. Journal of Agricultural and Food Chemistry, 51, 571–581. https://doi.org/10.1021/jf020926l.
35. Shi, Q., Lu, S., Li, D., Lu, J., Zhou, L., & Qiu, M. (2020). Cycloartane triterpene glycosides from rhizomes of Cimicifuga foetida L. with lipid-lowering activity on 3T3-L1 adipocytes. Fitoterapia, 145, 104635. https://doi.org/10.1016/j.fitote.2020.104635
36. Sun, B., Ricardo-da-Silva, J.M., & Spranger, I. (1998). Critical factors of vanillin assay for catechins and proanthocyanidins. Journal of Agricultural and Food Chemistry, 46, 4267–4274. https://doi.org/10.1021/jf980366j
37. Tamura, M. (1995). Ranunculaceae. In: Hiepko, P. (Ed.), Die Natürlichen Pflanzenfamilien, second ed., vol. 17a IV. Duncker and Humblot, Berlin, pp. 223–555.
38. Vasco, C., Ruales, J., & Kamal-Eldin, A. (2008). Total phenolic compounds and antioxidant capacities of major fruits of Ecuador. Food Chemistry, 111(4), 816–823. https://doi.org/10.1016/j.foodchem.2008.04.054
39. Wang, W., Li, R.Q., & Chen, Z.D. (2005). Systematic position of Asteropyrum (Ranunculaceae) inferred from chloroplast and nuclear sequences. Plant Systematics and Evolution, 255, 41–54. https://doi.org/10.1007/s.00606-005-0339-z
40. Xiang, K.L., & Wang, W. (2018). Actaea . In: A Dictionary of the Families and Genera of Chinese Vascular Plants ; Li, D.Z. Z., Ed.; Science Press Beijing, China; p 7.
41. Yuan, Q., & Yang, Q.E. (2006). Tribal relationships of Beesia, Eranthis and seven other genera of Ranunculaceae: Evidence from cytological characters. Botanical Journal of the Linnean Society, 150, 267–289. https://doi.org/10.1111/j.1095-8339.2006.0047.x
42. Zhang, H.Z., Guan, Z.X., & Wang, J.L. (1998). A study on edible wild vegetable resources and their exploitation and utilization in China. Resources Science, 20, 53–58.