Phytochemical profiles, antioxidant and antimicrobial activity of Actinidia polygama and A. arguta fruits and leaves

  • N. O. Khromykh Oles Honchar Dnipro National University
  • Y. V. Lykholat Oles Honchar Dnipro National University
  • O. O. Didur Oles Honchar Dnipro National University
  • T. V. Sklyar Oles Honchar Dnipro National University
  • V. R. Davydov Oles Honchar Dnipro National University
  • K. V. Lavrentievа Oles Honchar Dnipro National University
  • T. Y. Lykholat Oles Honchar Dnipro National University
Keywords: kiwiberry; secondary metabolites; GC-MS assay; bioactivity

Abstract

Plants of two species of Actinidia genus grown in an adverse steppe climate were examined in terms of secondary metabolites’ accumulation, antioxidant potential, and antimicrobial ability. The aim of the work was to reveal whether the introduced plants A. arguta and A. polygama retain their well-known health benefits. Total content of polyphenols (549.2 and 428.1 mg GAE/100 g FW, respectively), flavonoids, and phenolic acids as well as total antioxidant activity and reducing power of the fruit isopropanol extracts were found to be equal or even higher than the reported data on kiwifruit varieties cultivated in China and other regions. Antioxidant potential and phenolic compounds’ content in the fruit peel of both species were higher when compared to pulp, while corresponding indices of leaves exceeded those of the fruit. Disc-diffusion assays showed low to moderate antibacterial activity of A. arguta and A. polygama fruit and leaf extracts against collection Gram-negative and Gram-positive strains. Clinical strains of P. aeruginosa and E. coli resistant to the action of ofloxacin were notably inhibited by A. arguta and A. polygama fruit and leaf crude extracts. Inhibiting effects of plant extracts on clinical strains of K. pneumoniae and A. baumannii were comparable with the effect of ofloxacin. GC-MS assays identified 23 and 36 chemical constituents, respectively in A. arguta and A. polygama fruit isopropanol extracts. The main compounds in both extracts were 2-propenoic acid, pentadecyl ester followed by squalene, 7,9-di-tert-butyl-1-oxaspiro(4,5)deca-6,9-dien-2,8-dione, octadecanoic acid, 2-oxo-methyl ester, ethyl-isoallocholate, and phytol having known bioactivities. Our findings confirmed the preservation of useful properties by the introduced plants and also indicated the rich health-promoting abilities and expedience of cultivating A. arguta and A. polygama in a steppe climate.

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.

Alim, A., Li, T., Nisar, T., Ren, D., Zhai, X., Pang, Y., & Yang, X. (2019). Antioxidant, antimicrobial, and antiproliferative activitybased comparative study of peel and flesh polyphenols from Actinidia chinensis. Food and Nutrition Research, 63, 1577.

An, X., Lee, S. G., Kang, H., Heo, H. J., Cho, Y. S., & Do, K. (2016). Antioxidant and anti-inflammatory effects of various cultivars of kiwi berry (Actinidia arguta) on lipopolysaccharide-stimulated RAW 264.7 cells. Journal of Microbiology and Biotechnology, 26(8), 1367–1374.

Atkinson, R. G., & Macrae, E. A. (2007). Kiwifruit. In: Pua, E. C., & Davey, M. R. (Eds.). Transgenic crops V. Biotechnology in agriculture and forestry, vol. 60. Springer, Berlin, Heidelberg. Pp. 329–346.

Baranowska-Wójcik, E., & Szwajgier, D. (2019). Characteristics and pro-health properties of mini kiwi (Actinidia arguta). Horticulture, Environment, and Biotechnology, 60, 217–225.

Bekhradnia, S., Nabavi, S. M., Nabavi, S. F., & Ebrahimzadeh, M. A. (2011). Antioxidant activity of kiwifruit (Actinidia chinensis). Pharmacologyonline, 1, 758–764.

Bharathy, V., Sumathy, B., & Uthayakumari, F. (2012). Determination of phytocomponents by GC-MS in leaves of Jatropha gossypifolia L. Science Research Reporter, 2(3), 286–290.

Bhimba, B. V., Pushpam, A. C., Arumugam, P., & Prakash, S. (2012). Phthalate derivatives from the marine fungi Phoma herbarum VB7. International Journal of Biological and Pharmaceutical Research, 3(4), 507–512.

Cesoniene, L., Daubaras, R., Bogacioviene, S., Maruska, A. S., Stankevicius, M., Valatavicius, A., Zych, M., Ercisli, S., & Ilhan, G. (2020). Investigations of volatile organic compounds in berries of different Actinidia kolomikta (Rupr. & Maxim.) Maxim. accessions. Polish Journal of Food and Nutrition Sciences, 70(3), 291–300.

Deng, J. J., Yang, H. X., Fan, D. D., Cao, W., & Luo, Y. E. (2013). Antibacterial activities of polyphenolic extract from kiwi fruit (Actinidia chinensis Planch.) seeds. Journal of Pure and Applied Microbiology, 7(1), 491–494.

D'Evoli, L., Moscatello, S., Lucarini, M., Aguzzi, A., Gabrielli, P., Proietti, S., Battistelli, A., Famiani, F., & Lombardi-Boccia, G. (2015). Nutritional traits and antioxidant capacity of kiwifruit (Actinidia deliciosa Planch., cv. Hayward) grown in Italy. Journal of Food Composition and Analysis, 37, 25–29.

Dias, M., Caleja, C., Pereira, C., Calhelha, R. C., Kostic, M., Sokovic, M., Tavares, D., Baraldi, I. J., Barros, L., & Ferreira, I. C. F. R. (2020). Chemical composition and bioactive properties of byproducts from two different kiwi varieties. Food Research International, 127, 108753.

Drummond, L. (2013). Chapter Three – The composition and nutritional value of kiwifruit. In: Boland, M., & Moughan, P. J. (Eds.). Advances in food and nutrition research. Elsevier. Vol. 68. Pp. 33–57.

Du, G. R., Li, M. J., Ma, F. W., & Liang, D. (2009). Antioxidant capacity and the relationship with polyphenol and vitamin C in Actinidia fruits. Food Chemistry, 113(2), 557–562.

Gawron-Gzella, A., Dudek-Makuch, M., & Matlawska, I. (2012). DPPH radical scavenging activity and phenolic compound content in different leaf extracts from selected blackberry species. Acta Biologica Cracoviensia, Series Botanica, 54(2), 32–38.

He, X., Fang, J., Chen, X., Zhao, Z., Li, Y., Meng, Y., & Huang, L. (2019). Actinidia chinensis Planch.: A review of chemistry and pharmacology. Frontiers in Pharmacology, 10, 1236.

Huang, H. W., & Ferguson, A. R. (2007). Actinidia in China: Natural diversity, phylogeographical evolution, interspecific gene flow and kiwifruit cultivar improvement. Acta Horticulturae, 753, 31–40.

Jun, L., Stefan, W., & Chunlin, X. (2015). A review of bioactive plant polysaccharides: Biological activities, functionalization, and biomedical application. Bioactive Carbohydrates and Dietary Fibre, 5(1), 31–61.

Kannan, K., & Kannan, V. R. (2019). Characterization of the bioactive metabolite from a plant growth promoting rhizobacteria Pseudomonas aeruginosa VRKK1 and exploitation of antibacterial behaviour against Xanthomonas campestris a causative agent of bacterial blight disease in cowpea. Archives of Phytopathology and Plant Protection, 2019, 1–18.

Kim, J. G., Beppu, K., & Kataoka, I. (2009). Varietal differences in phenolic content and astringency in skin and flesh of hardy kiwifruit resources in Japan. Scientia Horticulturae, 120(4), 551–554.

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.

Latocha, P. (2017). The nutritional and health benefits of kiwi berry (A. arguta) – A review. Plant Foods for Human Nutrition, 72, 325–334.

Lee, I., Im, S., Jin, C.-R., Heo, H. J., Cho, Y.-S., Baik, M.-Y., & Kim, D.-O. (2015). Eeffect of maturity stage at harvest on antioxidant capacity and total phenolics in kiwifruits (Actinidia spp.) grown in Korea. Horticulture, Environment, and Biotechnology, 56(6), 841–848.

Leontowicz, H., Leontowicz, M., Latocha, P., Jesion, I., Park, Y.-S., Katrich, E., Barasch, D., Nemirovski, A., & Gorinstein, S. (2016). Bioactivity and nutritional properties of hardy kiwi fruit Actinidia arguta in comparison with Actinidia deliciosa 'Hayward' and Actinidia eriantha 'Bidan'. Food Chemistry, 196, 281–291.

Li, D., & Zhu, F. (2019). Physicochemical, functional and nutritional properties of kiwifruit flour. Food Hydrocolloids, 92, 250–258.

Lykholat, Y. V., Khromykh, N. O., Lykholat, T. Y., Didur, O. O., Lykholat, O. A., Legostaeva, T. V., Kabar, A. M., Sklyar, T. V., Savosko, V. M., Kovalenko, I. M., Davydov, V. R., Bielyk, Y. V., Volyanik, K. O., Onopa, A. V., Dudkina, K. A., & Grygoryuk, I. P. (2019). Industrial characteristics and consumer properties of Chaenomeles Lindl. fruits. Ukrainian Journal of Ecology, 9(3), 132–139.

Lykholat, Y. V., Khromykh, N. O., Didur, O. O., Drehval, O. A., Sklyar, T. V., & Anishchenko, A. O. (2021). Chaenomeles speciosa fruit endophytic fungi isolation and characterization of their antimicrobial activity and the secondary metabolites composition. Beni-Suef University Journal of Basic and Applied Sciences, 10, 83.

Merlin, N. J., Parthasarathy, V., Manavalan, R., & Kumaravel, S. (2009). Chemical investigation of aerial parts of Gmelina asiatica Linn by GC-MS. Pharmacognosy Research, 1(3), 152–156.

McGhie, T. K. (2013). Chapter Six – Secondary metabolite components of kiwifruit. Advances in Food and Nutrition Research, 68, 101–124.

Mikami-Konishide, I., Murakami, S., Nakanishi, K., Takahashi, Y., Yamaguchi, M., Shioya, T., Watanabe, J., & Hino, A. (2013). Antioxidant capacity and polyphenol content of extracts from crops cultivated in Japan, and the effect of cultivation environment. Food Science and Technology Research, 19(1), 69–79.

Mujeeb, F., Bajpai, P., & Pathak, N. (2014). Phytochemical evaluation, antimicrobial activity, and determination of bioactive components from leaves of Aegle marmelos. BioMed Research International, 2014, 497606.

Muthukrishnan, S., & Thinakaran, R. T. (2012). In silico exploration of anti-inflammatory activity of Pseudarthria viscida root. International Journal of Research in Pharmaceutical Sciences, 3(4), 517–520.

Oh, K.-K., Adnan, M., & Cho, D.-H. (2021). Network pharmacology-based study to uncover potential pharmacological mechanisms of Korean thistle (Cirsium japonicum var. maackii (Maxim.) Matsum.) flower against cancer. Molecules, 26(19), 5904.

Pal, R. S., Kumar, V. A., Arora, S., Sharma, A. K., Kumar, V., & Agrawal, S. (2015). Physicochemical and antioxidant properties of kiwifruit as a function of cultivar and fruit harvested month. Brazilian Archives of Biology and Technology, 58(2), 262–271.

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

Pinto, D., Sut, S., Dall’Acqua, S., Delerue-Matos, C., & Rodrigues, F. (2021). Actinidia arguta pulp: Phytochemical composition, radical scavenging activity, and in vitro cells effects. Chemistry and Biodiversity, 18(3), e2000925.

Prieto, P., Pineda, M., & Aguilar, M. (1999). Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: Specific application to the determination of vitamin E. Analytical Biochemistry, 269(2), 337–341.

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.

Salama, Z. A., Aboul-Enein, A. M., Gaafar, A. A., Abou-Elella, F., Aly, H. F., Asker, M. S., & Ahmed, H. A. (2018). Active constituents of kiwi (Actinidia deliciosa Planch) peels and their biological activities as antioxidant, antimicrobial and anticancer. Research Journal of Chemistry and Environment, 22(9), 52–59.

Satpal, D., Kaur, J., Bhadariya, V., & Sharma, K. (2021). Actinidia deliciosa (kiwi fruit): A comprehensive review on the nutritional composition, health benefits, traditional utilization, and commercialization. Journal of Food Processing and Preservation, 45(6), e15588.

Sosa, A. A., Bagi, S. H., & Hameed, I. H. (2016). Analysis of bioactive chemical compounds of Euphorbia lathyrus using gas chromatography-mass spectrometry and Fourier-transform infrared spectroscopy. Journal of Pharmacognosy and Phytotherapy, 8(5), 109–126.

Slinkard, K., & Singleton, V. L. (1977). Total phenol analysis: Automation and comparison with manual methods. American Journal of Enology and Viticulture, 28, 49–55.

Wang, M. Y., Macrae, E. A., Wohlers, M., & Marsh, K. (2011). Changes in volatile production and sensory quality of kiwifruit during fruit maturation in Actinidia deliciosa ‘Hayward’ and A. chinensis ‘Hort16A’. Postharvest Biology and Technology, 59(1), 16–24.

Wang, Y., Li, L., Liu, H., Zhao, T., Meng, C., Liu, Z., & Liu, X. (2018a). Bioactive compounds and in vitro antioxidant activities of peel, flesh and seed powder of kiwi fruit. International Journal of Food Science and Technology, 53(9), 2239–2245.

Wang, Y., Zhao, C.-L., Li, J.-Y., Liang, Y.-J., Yang, R.-Q., Liu, J.-Y., Ma, Z., & Wu, L. (2018b). Evaluation of biochemical components and antioxidant capacity of different kiwifruit (Actinidia spp.) genotypes grown in China. Biotechnology and Biotechnological Equipment, 32(3), 558–565.

Wei, L. B., Ma, S. Y., Liu, H. X., Huang, C. S., & Liao, N. (2018). Cytotoxic triterpenoids from roots of Actinidia chinensis. Chemistry and Biodiversity, 15(2), e1700454.

Williams, M. H., Boyd, L. M., McNeilage, M. A., MacRae, E. A., Ferguson, A. R., Beatson, R. A., & Martin, P. J. (2003). Development and commercialization of ‘Baby Kiwi’ (Actinidia arguta Planch). Acta Horticulturae, 610, 81–86.

Wojdyło, A., & Nowicka, P. (2019). Anticholinergic effects of A. arguta fruits and their polyphenol content determined by liquid chromatography-photodiode array detector quadrupole/time of flight-mass spectrometry (LC-MS-PDA-Q/TOF). Food Chemistry, 271(15), 216–223.

Xu, Y. X., Xiang, Z. B., Jin, Y. S., Shen, Y., & Chen, H. S. (2010). Two new triterpenoids from the roots of Actinidia chinensis. Fitoterapia, 81(7), 920–924.

Zhang, J., Tian, J., Gao, N., Gong, E. S., Xin, G., Liu, C., Si, X., Sun, X., & Li, B. (2021). Assessment of the phytochemical profile and antioxidant activities of eight kiwi berry (Actinidia arguta (Siebold & Zuccarini) Miquel) varieties in China. Food Science and Nutrition, 9(10), 5616–5625.

Zuo, L.-L., Wang, Z.-Y., Fan, Z.-L., Tian, S.-Q., & Liu, J.-R. (2012). Evaluation of antioxidant and antiproliferative properties of three Actinidia (Actinidia kolomikta, Actinidia arguta, Actinidia chinensis) extracts in vitro. International Journal of Molecular Sciences, 13(5), 5506–5518.

Published
2022-02-11
Section
Articles