Variability of the antioxidant properties of Berberis fruits depending on the plant species and conditions of habitat

  • N. O. Khromykh Oles Honchar Dnipro National University
  • Y. V. Lykholat Oles Honchar Dnipro National University
  • I. M. Kovalenko Sumy’ National Agricultural University
  • A. M. Kabar Oles Honchar Dnipro National University
  • O. O. Didur Oles Honchar Dnipro National University
  • M. I. Nedzvetska Oles Honchar Dnipro National University
Keywords: fruit plants; Berberis; antioxidants; phenols; flavonoids; total reducing power

Abstract

Plant fruits, leaves, stems, and other parts are of high nutritional value, and are the source of physiologically active compounds, which can contribute to the treatment of many diseases caused by oxidative stress. Enrichment of the species spectrum of the fruit plants expands the possibilities of their use in dietary nutrition and human treatment. Unfortunately, the introduction of the new fruit plant species in industrial gardens in the Steppe Dnieper is limited to a large extent by the unfavorable climate. In this regard, the assessment of the possibility of realizing the genetic potential of fruit plants from different geographical areas in the steppe climate acquires both scientific and practical significance. The study was conducted on the basis of the fruit plants collection collection of the Botanical Garden of the DNU including four introduced species and one natural species from the genus Berberis. The anomalous weather conditions during the growing season of 2017 (snowfall in April followed by a drought in June) were accompanied by an earlier stage appearance of leaves, flowering and fruit ripening of all introduced plants, especially the Asian species B. amurensis and B. koreana, compared to the native species B. vulgaris. In accordance with the results obtained, fresh weight of the ripe fruits of Berberis species decreased in the order of B. amurensis > B. vulgaris > B. canadensis > B. koreana > B. x declinata. The highest total phenolics content, determined in the isopropanolic fruit extracts by Folin – Ciocalteau assay, was found in the fresh ripe fruits of B. koreana (1362 ± 66 mg GAE/100 g WW), followed by B. x declinata and B. vulgaris fruits (91% and 77% of the B. koreana phenolics content respectively). The highest total flavonoids content determined using the aluminum chloride method was revealed in the fruits of B. koreana (210 ± 6 mg RE/100 g FW) exceeding the content in fruits of other Berberis species by 1.1–2.1 times, while the lowest value (103 ± 4 mg RE/100 g FW) was found in the fruits of B. amurensis. The total reducing power, determined by RP assay, varied in the range from 5.0 to 9.6 mg AAE/100 g DW, and the highest levels were found in the fruits of B. koreana and B. x declinata (respectively, 9.6 ± 0.6 and 8.6 ± 0.5 mg AE/100 g DW) exceeding the reducing capacity of other Berberis species by 1.7–1.9 times. In the fruits of genus Berberis species strong positive correlation was found between the total reducing power and the total content of phenols (r = 0.87), as well as between the reducing power and the total content of flavonoids (r = 0.84). High correlation coefficients confirm the significant contribution of the Berberis fruit phenolic compounds, including the flavonoids, to the antioxidant capacity. So, the study results showed that fruits of all examined Berberis species can be an easily accessible source of antioxidants, however, the antioxidant capacity of fruits decreased in order of B. koreana > B. x declinata > B. vulgaris > B. amurensis > B. canadensis.

References

Abd El-Wahab, A. E., Ghareeb, D. A., Sarhan, E. E. M., Abu-Serie, M. M., & El Demellawy, M. A. (2013). In vitro biological assessment of Berberis vulgaris and its active constituent, berberine: antioxidants, anti-acetylcholinesterase, anti-diabetic and anticancer effects. BMC Complementary and Alternative Medicine, 13, 218.


Andola, H. C., Gaira, K. S., Rawal, R. S., Rawat, M. S., & Bhatt, I. D. (2010). Habitat-dependent variations in berberine content of Berberis asiatica Roxb. ex. DC. in Kumaon, Western Himalaya. Chemistry and Biodiversity, 7(2), 415–420.


Augustus, O. K., Janet, J. O., Ebenezer, T. B., & Ogboma, U. J. (2015). Antioxidant activities, total flavonoid and total phenolic contents of whole plant of Kyllinga erecta Shumach. Journal of Food and Nutrition Research, 3(8), 489–494.


Bak, I., Lekli, I., Juhasz, B., Varga, E., Varga, B., Gesztelyi, R., Szendrei, L., & Tosaki, A. (2010). Isolation and analysis of bioactive constituents of sour cherry (Prunus cerasus) seed kernel: An emerging functional food. Journal of Medicinal Food, 13(4), 905–910.


Bettaieb, I., Knioua, S., Hamrouni, I., Limam, F., & Marzouk, B. (2011). Water-deficit impact on fatty acid and essential oil composition and antioxidant activities of cumin (Cuminum cyminum L.) aerial parts. Journal of Agricultural and Food Chemistry, 59(1), 328–334.


Bonesi, M., Loizzo, M. R., Conforti, F., Passalacqua, N. G., Saab, A., Menichini, F., & Tundis, R. (2013). Berberis aetnensis and B. libanotica: A comparative study on the chemical composition, inhibitory effect on key enzymes linked to Alzheimer’s disease and antioxidant activity. Journal of Pharmacy and Pharmacology, 65(12), 1726–1735.


Borges, G., Degeneve, A., Mullen, W., & Crozier, A. (2010). Identification of Flavonoid and phenolic antioxidants in black currants, blueberries, raspberries, red currants, and cranberries. Journal of Agricultural and Food Chemistry, 58(7), 3901–3909.


Brewer, M. S. (2011). Natural antioxidants: Sources, compounds, mechanisms of action, and potential applications. Comprehensive Reviews in Food Science and Food Safety, 10, 221–247.


Brygadyrenko, V. V. (2015). Community structure of litter invertebrates of forest belt ecosystems in the Ukrainian Steppe Zone. International Journal of Environmental Research, 9(4), 1183–1192.


Deepa, G., Ayesha, S., Nishtha, K., & Thankamani, M. (2013). Comparative evaluation of various total antioxidant capacity assays applied to phytochemical compounds of Indian culinary spice. International Food Research Journal, 20(4), 1711–1716.


Di, D. L., Liu, Y. W., Ma, Z. G., & Jiang, S. X. (2003). Determination of four alkaloids in Berberis plants by HPLC. Zhongguo Zhong Yao Za Zhi, 28(12), 1132–1134 (in Chinese).


Eghdami, A., Eizadi, M., & Sadeghi, F. (2013). Polyphenolic content and antioxidant activity of hydroalcohlic and alcoholic extract of Thymus vulgaris. Journal of Biodiversity and Environmental Sciences, 3(5), 94–101.


Eghdami, A., & Sadeghi, F. (2010). Determination of total phenolic and flavonoids contents in methanolic and aqueous extract of Achillea millefolium. The Journal of Organic Chemistry, 2, 81–84.


Habtemariam, S. (2011). The therapeutic potential of Berberis darwinii stem-bark: Quantification of berberine and in vitro evidence for Alzheimer’s disease therapy. Natural Product Communications, 6(8), 1089–1090.


Hoshyar, R., Mahboob, Z., & Zarban, A. (2016). The antioxidant and chemical properties of Berberis vulgaris and its cytotoxic effect on human breast carcinoma cells. Cytotechnology, 68, 1207–1213.


Huang, W. Y., Cai, Y. Z., & Zhang, Y. (2010). Natural phenolic compounds from medicinal herbs and dietary plants: Potential use for cancer prevention. Nutrition and Cancer, 62(1), 1–20.


Imanshahidi, M., & Hosseinzadeh, H. (2008). Pharmacological and therapeutic effects of Berberis vulgaris and its active constituent, berberine. Phytotherapy Research, 22(8), 999–1012.


Imenshahidi, M., & Hosseinzadeh, H. (2016). Berberis vulgaris and berberine: An update review. Phytotherapy Research, 30(11), 1745–1764.


Jafari, S., Saeidnia, S., & Abdollahi, M. (2014). Role of natural phenolic compounds in cancer chemoprevention via regulation of the cell cycle. Current Pharmaceutical Biotechnology, 15(4), 409–421.


Ji, H. F., & Shen, L. (2011). Berberine: A potential multipotent natural product to combat Alzheimer’s disease. Molecules, 16(8), 6732–6740.


Kaldmae, H., Kikas, A., Arus, L., & Libek, A.-V. (2013). Genotype and microclimate conditions influence ripening pattern and quality of blackcurrant (Ribes nigrum L.) fruit. Zemdirbyste-Agriculture, 100(2), 167–174.


Koncić, Z. M., Kremer, D., Karlović, K., & Kosalec, I. (2010). Evaluation of antioxidant activities and phenolic content of Berberis vulgaris L. and Berberis croatica Horvat. Food and Chemical Toxicology, 48(8–9), 2176–2180.


Kul’bachko, Y., Loza, I., Pakhomov, O., & Didur, O. (2011). The zooecological remediation of technogen faulted soil in the industrial region of the Ukraine steppe zone. In: Behnassi, M., Shahid, S., & D’Silva, J. (Eds.). Sustainable agricultural development. Springer, Dordrecht.


Lakache, Z., Tigrine-Kordjani, N., Tigrine, C., Aliboudhar, H., & Kameli, A. (2016). Phytochemical screening and antioxidant properties of methanolic extract and different fractions of Crataegus azarolus leaves and flowers from Algeria. International Food Research Journal, 23(4), 1576–1583.


Lavola, A., Karjalainen, R., & Julkunen-Tiitto, R. (2012). Bioactive polyphenols in leaves, stems, and berries of saskatoon (Amelanchier alnifolia Nutt.) cultivars. Journal of Agricultural and Food Chemistry, 60, 1020–1027.


Lykholat, T., Lykholat, O., & Antonyuk, S. (2016). Immunohistochemical and biochemical analysis of mammary gland tumours of different age patients. Cytology and Genetics, 50(1), 32–41.


Lykholat, Y. V., Khromykh, N. A., Ivan’ko, I. A., Matyukha, V. L., Kravets, S. S., Didur, O. O., Alexeyeva, A. A., & Shupranova, L. V. (2017). Otsinka i prohnoz invaziinosti deiakykh adventyvnykh roslyn za vplyvu klimatychnykh zmin u Stepovomu Prydniprov’i [Assessment and prediction of the invasiveness of some alien plants in conditions of climate change in the steppe Dnieper region]. Biosystems Diversity, 25(1), 52–59.


McGhie, T. K., Hunt, M., & Barnett, L. E. (2005). Cultivar and growing region determine the antioxidant polyphenolic concentration and composition of apples grown in New Zealand. Journal of Agricultural and Food Chemistry, 53(8), 3065–3070.


Moyer, R. A., Hummer, K. E., Finn, C. E., Frei, B., & Wrolstad, R. E. (2002). Anthocyanins, phenolics, and antioxidant capacity in diverse small fruits: Vaccinium, Rubus, and Ribes. Journal of Agricultural and Food Chemistry, 50(3), 519–525.


Nichols, S. N., Hofmann, R. W., & Williams, W. M. (2015). Functional roles of secondary metabolites in plant-environment interactions. Physiological drought resistance and accumulation of leaf phenolics in white clover interspecific hybrids. Environmental and Experimental Botany, 119, 40–47.


Nwanna, E. E., Ibukun, E. O., & Oboh, G. (2013). Inhibitory effects of methanolic extracts of two eggplant species from South-Western Nigeria on starch hydrolysing enzymes linked to type-2 diabetes. African Journal of Pharmacy and Pharmacology. 7(23), 1575–1584.


Orhan, I. E. (2012). Current concepts on selected plant secondary metabolites with promising inhibitory effects against enzymes linked to Alzheimer’s disease. Current Medicinal Chemistry, 19(14), 2252–2261.


Pękal, A., & Pyrzynska, K. (2014). Evaluation of aluminium complexation reaction for flavonoid content assay. Food Analytical Methods, 7, 1776–1782.


Pulido, R., Bravo, R. L., & Saura-Calixto, F. (2000). Antioxidant activity of dietary polyphenols as determined by a modified ferric reducing/antioxidant power assay. Journal of Agricultural and Food Chemistry, 48, 3396–3402.


Pyrkosz-Biardzka, K., Kucharska, A. Z., Sokół-Łętowska, A., Strugała, P., & Gabrielska, J. (2014). A comprehensive study on antioxidant properties of crude extracts from fruits of Berberis vulgaris L., Cornus mas L. and Mahonia aquifolium Nutt. Polish Journal of Food and Nutrition Sciences, 64(2), 91–99.


Rahimi-Madiseh, M., Lorigoini, Z., Zamani-Gharaghoshi, H., & Rafieian-Kopaei, M. (2017). Berberis vulgaris: Specifications and traditional uses. Iranian Journal of Basic Medical Sciences, 20, 569–587.


Sahan, Y., Cansev, A., Celik, G., & Cinar, A. (2012). Determination of various chemical properties, total phenolic content, antioxidant capacity and organic acids in Laurocerasus officinalis fruits. Acta Horticulturae, 939, 359–366.


Shcherbyna, R. O., Danilchenko, D. M., Parchenko, V. V., Panasenko, O. I., Knysh, E. H., Hromyh, N. A., & Lyholat, Y. V. (2017). Study of 2-((5-R-4-R1-4h-1,2,4-Triazole-3-YI0Thio)acetic acid salts on growth and progress of blackberries (Kiowa variety) propagules. Research Journal of Pharmaceutical, Biological and Chemical Sciences, 8(3), 975–979.


Singleton, V. L., Orthofer, R., & Lamuela-Raventos, R. M. (1999). Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteau reagent. Methods in Enzymology, 299, 152–178.


Tomosaka, H., Chin, Y. W., Salim, A. A., Keller, W. J., Chai, H., & Kinghorn, A. D. (2008). Antioxidant and cytoprotective compounds from Berberis vulgaris (barberry). Phytotherapy Research, 22(7), 979–981.


Vagiri, M., Ekholm, A., Öberg, E., Johansson, E., Andersson, S. C., & Rumpunen, K. (2013). Phenols and ascorbic acid in black currants (Ribes nigrum L.): Variation due to genotype, location, and year. Journal of Agricultural and Food Chemistry, 61(39), 9298–9306.


Wojdyło, A., Jáuregui, P. N. N., Carbonell-Barrachina, A. A., Oszmiański, J., & Golis, T. (2013). Variability of phytochemical properties and content of bioactive compounds in Lonicera caerulea L. var. kamtschatica Berries. Journal of Agricultural and Food Chemistry, 61(49), 12072–12084.


Wojdyło, A., Oszmiański, J., & Laskowski, P. (2008). Polyphenolic compounds and antioxidant activity of new and old apple varieties. Journal of Agricultural and Food Chemistry, 56(15), 6520–6530.


Wolfe, K., Wu, X., & Liu, R. H. (2003). Antioxidant activity of apple peels. Journal of Agricultural and Food Chemistry, 51(3), 609–614. 

Published
2018-02-09
How to Cite
Khromykh, N. O., Lykholat, Y. V., Kovalenko, I. M., Kabar, A. M., Didur, O. O., & Nedzvetska, M. I. (2018). Variability of the antioxidant properties of Berberis fruits depending on the plant species and conditions of habitat. Regulatory Mechanisms in Biosystems, 9(1), 56-61. https://doi.org/10.15421/021807

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