Interspecific differences of antioxidant ability of introduced Chaenomeles species with respect to adaptation to the steppe zone conditions


  • N. Khromykh Oles Honchar Dnipro National University
  • Y. Lykholat Oles Honchar Dnipro National University
  • L. Shupranova Oles Honchar Dnipro National University
  • A. Kabar Oles Honchar Dnipro National University
  • O. Didur Oles Honchar Dnipro National University
  • T. Lykholat Oles Honchar Dnipro National University
  • Y. Kulbachko Oles Honchar Dnipro National University
Keywords: Chaenomeles; fruits; leaves; antioxidant enzymes; phenols; flavonoids; total reducing power

Abstract

Plants of the genus Chaenomeles are traditionally used in the countries of South-East Asia, due to their high nutritional and health-promoting properties. However, the successful introduction of species promising for gardening from geographically remote areas requires the study of plant ontogeny under the conditions of new habitat. This is a very substantial problem for the steppe zone, where the continental climate has features of aridity and complicates the process of increasing the diversity of fruit crops by introducing the desired species. The present study aims to assess the effectiveness of the protective enzymatic system of different Chaenomeles genotypes subject to a steppe climate as well as the accumulation of the biologically active compounds with high antioxidant capacity. The study was performed on the basis of the introduced horticultural plants collection in the Botanical Garden of the DNU, and the Chaenomeles fruits, leaves, and the seeds were examined. The highest activity of catalase, benzidine-peroxidase and guaiacol-peroxidase, and the greatest enzymes activation during vegetation were found in leaves of Ch. cathayensis and Ch. speciosa, while the lowest activity was in leaves of both Japanese species. The biggest total phenolic content in the isopropanolic plant extracts, determined by Folin–Ciocalteau assay, was found in leaves of Ch. × superba, Ch. × californica and Ch. cathayensis (44.8, 52.8, and 43.6 mg GAE/g WW); a less high level was found in leaves of Ch. japonica and Ch. japonica var. maulei (43.1 and 40.2 mg GAE/g), while the lowest was in leaves of Ch. speciosa (29.3 mg GAE/g). The total flavonoids content determined using the aluminum chloride method, did not differ by variety or species in the plant leaves, being in the range of 2.6–2.9 mg of RE per g WW (accordingly, in leaves of Ch. japonica var. maulei and Ch. × californica). The high total reducing power determined by potassium ferricyanide assay was found in leaves of both hybridogenic species and Ch. cathayensis (respectively, 11.6, 14.1, and 11.4 AAE/g WW); leaves of both Japanese species had slightly lower values and the lowest was in leaves of Ch. speciosa (7.7 AAE/g). In the Chaenomeles fruits, the total phenolic content was the lowest in Ch. speciosa (17.8 mg GAE/g), average in both Japanese species (28.7 and 27.8 mg GAE/g), and the highest (33.3 mg GAE/g) was in Ch. cathayensis. The flavonoid accumulation was highest in the fruits of Ch. cathayensis and Ch. japonica var. maulei (0.67 and 0.63 mg RE/g), intermediate in both hybridogenic species and Ch. japonica (accordingly, 0.57, 0.42 and 0.38 mg RE/g), and the lowest in Ch. speciosa (0.30 mg RE/g). The total reducing power of Chaenomeles fruit was lower as compared to leaves, and decreased from 11.2 to 5.7 mg AAE/g in the series Ch. cathayensis > Ch. × californica > Ch. japonica > Ch. japonica var. maulei > Ch. × superba > Ch. speciosa. High correlation coefficients between total reducing power and total phenols content in the Chaenomeles leaves and fruits (respectively, r = 0.96 and r = 0.95, P < 0.05) confirm the significant contribution of phenolic compounds to the antioxidant capacity. The study results indicate a high antioxidant capacity of the Chaenomeles species in the conditions of the steppe climate due to the antioxidant enzymes activity and the accumulation of a significant amount of phenolic metabolites in leaves and fruits.

References


Alexeyeva, A. A., Lykholat, Y. V., Khromykh, N. O., Kovalenko, I. M., & Boroday, E. S. (2016). The impact of pollutants on the antioxidant protection of species of the genus Tilia at different developmental stages. Visnyk of Dnipropetrovsk University. Biology, Ecology, 24(1), 188–192.


Allison, S. D., & Schultz, J. C. (2004). Differential activity of peroxidase isozymes in response to wounding, gypsy moth, and plant hormones in Northern red oak (Quercus rubra L.). Journal of Chemical Ecology, 30(7), 1363–1379.


Arya, N., Prakash, O., Verma, A. K., & Pant, A. K. (2015). Variation in antioxidant potential of Curcuma longa L. collected from different ecological niches of Western Himalayan region. International Journal of Pharmacy and Pharmaceutical Sciences, 7(7), 85–90.


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.


Baranowska-Bosiacka, I., Bosiacka, B., Rast, J., Gutowska, I., Wolska, J., Rbacz-Maron, E., Dкbia, K., Janda, K., Korbecki, J., & Chlubek, D. (2017). Macro- and microelement content and other properties of Chaenomeles japonica L. fruit and protective effects of its aqueous extract on hepatocyte metabolism. Biological Trace Element Research, 178(2), 327–337.


Bartish, I. V., Garkava, L. P., Rumpunen, K., & Nybom, H. (2000). Phylogenetic relationships and differentiation among and within populations of Chaenomeles Lindl. (Rosaceae) estimated with RAPDs and isozymes. Theoretical and Applied Genetics, 101, 554–563.


Beecher, G. R. (2003). Overview of dietary flavonoids: Nomenclature, occurrence and intake. The Journal of Nutrition, 133(10), 3248S–3254S.


Bouterfas, K., Mehdadi, Z., Elaoufi, M. M., Latreche, A., & Benchiha, W. (2016). Antioxidant activity and total phenolic and flavonoids content variations of leaves extracts of white Horehound (Marrubium vulgare Linné) from three geographical origins. Annales Pharmaceutiques Francaises, 74(6), 453–462.


Brglez, M. E., Knez, H. M, Škerget, M., Knez, Ž., & Bren, U. (2016). Polyphenols: Extraction methods, antioxidative action, bioavailability and anticarcinogenic effects. Molecules, 21(7), e901.


Cheynier, V. (2005). Polyphenols in foods are more complex than often thought. The American Journal of Clinical Nutrition, 81(1), 223S–229S.


Costa, R. M., Magalhгes, A. S., Pereira, J. A., Andrade, P. B., Valentгo, P., Carvalho, M., & Silva, B. M. (2009). Evaluation of free radical-scavenging and antihemolytic activities of quince (Cydonia oblonga) leaf: A comparative study with green tea (Camellia sinensis). Food and Chemical Toxicology, 47(4), 860–865.


Du, H., Wu, J., Li, H., Zhong, P. X., Xu, Y. J., Li, C. H., Ji, K. X., & Wang, L. S. (2013). Polyphenols and triterpenes from Chaenomeles fruits: Chemical analysis and antioxidant activities assessment. Food Chemistry, 141(4), 4260–4268.


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.

Gorlach, S., Wagner, W., Podsкdek, A., Szewczyk, K., Kozioіkiewicz, M., & Dastych, J. (2011). Procyanidins from Japanese quince (Chaenomeles japonica) fruit induce apoptosis in human colon cancer Caco-2 cells in a degree of polymerization-dependent manner. Nutrition and Cancer, 63(8), 1348–1360.


Górnaś, P., Siger, A., Juhņeviča, K., Lācis, G., Šnē, E., & Segliņa, D. (2014). Cold-pressed Japanese quince (Chaenomeles japonica (Thunb.) Lindl. ex Spach) seed oil as a rich source of α-tocopherol, carotenoids and phenolics: A comparison of the composition and antioxidant activity with nine other plant oils. European Journal of Lipid Science and Technology, 116(5), 563–570.


Góth, L. (1991). A simple method for determination of serum catalase activity and revision of reference range. Clinica Chimica Acta, 196(2–3), 143–151.


Gregory, R. P. F. (1966). A rapid assay for peroxidase activity. Biochemical Journal, 101(3), 582–583.


Hafez-Taghva, P., Zamzad, M., & Khalafi, L. (2016). Total flavonoid content and essential oil composition of Chaenomeles japonica (Thunb.) Lindl. ex Spach from North of Iran. Indian Journal of Natural Products and Resources, 7(1), 90–92.


Halliwell, B. (2006). Reactive species and antioxidants. Redox biology is a fundamental theme in aerobic life. Plant Physiology, 141, 312–322.


Hamauzu, Y., Inno, T., Kume, C., Irie, M., & Hiramatsu, K. J. (2006). Antioxidant and antiulcerative properties of phenolics from Chinese quince, quince, and apple fruits. Journal of Agricultural and Food Chemistry, 54(3), 765–772.


Han, Y. K., Kim, Y. S., Natarajan, S. B., Kim, W. S., Hwang, J. W., Jeon, N. J., Jeong, J. H., Moon, S. H., Jeon B. T., & Park P. J. (2016). Antioxidant and anti-inflammatory effects of Chaenomeles sinensis leaf extracts on LPS-stimulated RAW 264.7 Cells. Molecules, 21(4), 422.


Huseynova, I. M., Aliyeva, D. R., Mammadov, A. C., & Aliyev, J. A. (2015). Hydrogen peroxide generation and antioxidant enzyme activities in the leaves and roots of wheat cultivars subjected to long-term soil drought stress. Photosynthesis Research, 125, 279–289.


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.


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.


Laemmly, U. K. (1970). Cleavage of structural of bacteriophage T-4. Nature, 227, 680–685.


Lee, B.-R., Kim, K.-Y., Jung, W.-J., Avice, J.-C., Ourry, A., & Kim, T.-H. (2007). Peroxidases and lignification in relation to the intensity of water-deficit stress in white clover (Trifolium repens L.). Journal of Experimental Botany, 58(6), 1271–1279.


Lewandowska, U., Szewczyk, K., Owczarek, K., Hrabec, Z., Podsкdek, A., Koziołkiewicz, M., & Hrabec, E. (2013). Flavanols from Japanese quince (Chaenomeles japonica) fruit inhibit human prostate and breast cancer cell line invasiveness and cause favorable changes in Bax/Bcl-2 mRNA ratio. Nutrition and Cancer, 65(2), 273–285.


Luna, C. M., Pastori, G. M., Driscoll, S., Groten, K., Bernard, S., & Foyer, C. H. (2005). Drought controls on H2O2 accumulation, catalase (CAT) activity and CAT gene expression in wheat. Journal of Experimental Botany, 56(411), 417–423.


Ma, B., Wang, J., Tong, J., Zhou, G., Chen, Y., He, J., & Wang, Y. (2016). Protective effects of Chaenomeles thibetica extract against carbon tetrachloride-induced damage via the MAPK/Nrf2 pathway. Food and Function, 7(3), 1492–1500.


Mcdonald, J. H. (2014). Handbook of biolological statistics. Sparky House Publishing, Baltimore.


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.


Miao, J., Zhao, C., Li, X., Chen, X., Mao, X., Huang, H., Wang, T., & Gao, W. (2016). Chemical composition and bioactivities of two common Chaenomeles fruits in China: Chaenomeles speciosa and Chaenomeles sinensis. Journal of Food Science, 81(8), H2049–2058.


Mitic, V., Ilic, M., Dimitrijevic, M., Cvetkovic, J., Ciric, S., & Stankov-Jovanovic, V. (2016). Chemometric characterization of peach, nectarine and plum cultivars according to fruit phenolic content and antioxidant activity. Fruits, 7(1), 57–66.


Mojzer, E. B., Hrnčič, M. K., Škerget, M., Knez, Ž., & Bren, U. (2016). Polyphenols: Extraction methods, antioxidative action, bioavailability and anticarcinogenic effects. Molecules, 21(7), e901.


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.


Owczarek, K., Hrabec, E., Fichna, J., Sosnowska, D., Koziołkiewicz, M., Szymański, J., & Lewandowska, U. (2017). Flavanols from Japanese quince (Chaenomeles japonica) fruit suppress expression of cyclooxygenase-2, etalloproteinase-9, and nuclear factor-kappaB in human colon cancer cells. Acta Biochimica Polonica, 64(3), 567–576.


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.


Radhika, V., & Rao, V. S. H. (2015). Computational approaches for the classification of seed storage proteins. Journal of Food Science and Technology, 52(7), 4246–4255.


Ranieri, A., Castagna, A., Baldam, B., & Soldatini, G. F. (2001). Iron deficiency differently affects peroxidase isoforms in sunflower. Journal of Experimental Botany, 52(354), 25–35.


Ros-García, J. M., Sánchez, J. L., Hellı́n, P., Jordán, M. J., Vila, R., Rumpunen, K. (2004). Characterization of juice in fruits of different Chaenomeles species. LWT-Food Science and Technology, 37(3), 301–307.


Rumpunen, K. (2002). Chaenomeles: Potential new fruit crop for Northern Europe. In: Janick, J., & Whipkey, A. (Eds.). Trends in new crops and new uses. ASHS Press, Alexandria. Pp. 385–392.


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.


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(3), 571–581.


Shcherbyna, R. O., Danilchenko, D. M., Parchenko, V. V., Panasenko, O. I., Knysh, E. H., Hromyh, N. A., & Lyholat, Y. V. (2017). Studying 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.


Strugała, P., Cyboran-Mikołajczyk, S., Dudra, A., Mizgier, P., Kucharska, A. Z., Olejniczak, T., & Gabrielska, J. (2016). Biological activity of japanese quince extract and its interactions with lipids, erythrocyte membrane, and human albumin. The Journal of Membrane Biology, 249(3), 393–410.


Suh, W. S., Park, K. J., Kim, D. H., Subedi, L., Kim, S. Y., Choi, S. U., & Lee, K. R. (2017). A biphenyl derivative from the twigs of Chaenomeles speciosa. Bioorganic Chemistry, 72, 156–160.


Vrhovsek, U., Rigo, A., Tonon, D., & Mattivi, F. (2004). Quantitation of polyphenols in different apple varieties. Journal of Agricultural and Food Chemistry, 52(21), 6532–6538.


Watychowicz, K., Janda, K., Jakubczyk, K., & Wolska, J. (2017). Chaenomeles – health promoting benefits. Roczniki Panstwowego Zakladu Higieny, 68(3), 217–227.


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.


Zakłos-Szyda, M., & Pawlik, N. (2018). Japanese quince (Chaenomeles japonica L.) fruit polyphenolic extract modulates carbohydrate metabolism in HepG2 cells via AMP-activated protein kinase. Acta Biochimica Polonica, 65(1), 67–78.


Zhang, S., Han, L., Zhang, H., & Xin, H. (2014). Chaenomeles speciosa: A review of chemistry and pharmacology. Biomedical Reports, 2(1), 12–18.


Published
2018-05-10
Section
Articles

Most read articles by the same author(s)