ACCUMULATION OF PHENOLICS IN ELEUTHERO (Eleutherococcus senticosus (Rupr. et Maxim.) Maxim.) AS AFFECTED BY PLANT DEVELOPMENT
Katarzyna Bączek
Warsaw University of Life Science – SGGW, Department of Vegetable and Medicinal Plants, Nowoursynowska 166, 02-787 Warsaw, PolandJarosław L. Przybył
Warsaw University of Life Science – SGGW, Department of Vegetable and Medicinal Plants, Nowoursynowska 166, 02-787 Warsaw, PolandOlga Kosakowska
Warsaw University of Life Science – SGGW, Department of Vegetable and Medicinal Plants, Nowoursynowska 166, 02-787 Warsaw, PolandZenon Węglarz
Warsaw University of Life Science – SGGW, Department of Vegetable and Medicinal Plants, Nowoursynowska 166, 02-787 Warsaw, PolandAbstract
The aim of the study was to determine the effect of plant age and growth phase on the accumulation of phenolics in stem bark, leaves and underground organs of Eleuthero. Their content was assessed using validated HPLC-DAD method. In underground organs and stem bark 7 phenolics were determined, i.e. eleutherosides
B and E as well as caffeic, ferulic, chlorogenic, rosmarinic and protocatechuic acids. The content of eleutherosides B was significantly higher in stem bark while eleutherosides E, in underground organs. Accumulation of these compounds was the highest in the 4-year-old plants (87.43 mg·100 g–1 DW of eleutherosides
B and 85.22 mg·100 g–1 DW of eleutherosides E in underground organs; 302.21 mg·100 g–1 DW of eleutherosides B and 24.89 mg·100 g–1 DW eleutherosides E in stem bark). In these organs, among identified phenolic acids chlorogenic acid was the dominant. In the leaves 4 phenolic acids (caffeic, ferulic, chlorogenic and rosmarinic acids), as well as 2 flavonoids (rutoside and hyperoside), were identified. Flavonoids and caffeic acid occurred in higher amounts at the beginning of leaf senescence, whereas the other phenolic acids – at the full vegetation. Their content was the highest in 2-year-old plants.
Keywords:
plant age, HPLC analysis, eleutherosides, phenolic acids, flavonoidsReferences
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Bączek, K., Banaszczak, P., Przybył, J.L., Węglarz, Z., Pelc, M. (2010). Charakterystyka chemiczna organów nadziemnych i podziemnych 8 gatunków z rodzaju Eleutheroccocus. Zesz. Probl. Post. Nauk. Rol., 555, 163–168.
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Deyama, T., Nishibe, S., Nakazawa, Y. (2001). Constituents and pharmacological effects of Eucommia and Siberian ginseng. Acta Pharmacol. Sin., 22, 1057–1070.
EMA (European Medicines Agency) (2014). Assessment report on Eleutherococcus senticosus (Rupr.et Maxim.) Maxim., radix EMA/HMPC/680615/2013.
Erlejman, A.G., Verstraeten, S.V., Fraga, C.G., Oteiza, P.I. (2004). The interaction of flavonoids with membranes: potential determinant of flavonoid antioxidant effects. Free Radic. Res., 38(12), 1311–1320.
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Falé, P.L., Borges, C., Madeira, P.J.A., Ascensão, L., Araújo, M.E.M, Florêncio, M.H, Serralheiro, M.L.M. (2009). Rosmarinic acid, scutellarein 40-methyl ether 7-O-glucuronide and (16S)-coleon E are the main compounds responsible for the antiacetylcholinesterase and antioxidant activity in herbal tea of Plectranthus barbatus („falso boldo”). Food Chem., 114, 798–805.
Glazener, J.A. (1982). Accumulation of phenolic compounds in cells and formation of lignin-like polymers in cell walls of young tomato fruits after inoculation with Botrytis cinerea. Physiol. Plant Pathol., 20, 11–25.
Gong, X., Zhang, L., Jiang, R., Wang, C.D., Yin, X.R., Wan, J.Y. (2013). Hepatoprotective effects of syringin on fulminant hepatic failure induced by D-galactosamine and lipopolysaccharide in mice. J. Appl. Toxicol., 34, 265–271.
Gűlçin, I. (2006). Antioxidant activity of caffeic acid (3,4-dihydroxycinnamic acid). Toxicol., 217, 213–220.
Huang, L.Z., Wei, L., Zhao, H.F., Huang, B.K., Rahman, K., Qin, L.P. (2011). The effect of Eleutheroside E on behavioral alterations in murine sleep deprivation stress model. Eur. J. Pharmacol., 658, 150–155.
Inderjit, S., Streibig, J.C., Olofsdotter, M. (2002). Joint action of phenolic acid mixtures and its significance in allelopathy research. Physiol. Plant., 114, 422–428.
Kakkar, S., Bais, S.A. (2014). Review on protocatechuic acid and its pharmacological potential. ISRN Pharmacol., ID: 952943.
Kim, C.H., Sun, B.Y. (2004). Infrageneric classification of the genus Eleutherococcus Maxim. (Araliaceae) with a new section Cissiflolius. J. Plant Biol., 47, 282–288.
Kim, Y.H., Bae, D.B., Lee, J.S., Park, S.O., Lee, S.J., Cho, O.H., Lee, O.H. (2013). Determination of eleuthero-sides and β-glucan content from different parts and cultivating areas of A. senticosus and A. koreanum. J. Korean Soc. Food Sci. Nutr., 42, 2082–2087.
Kim, Y.H., Cho, M.L., Kim, D., Shin, G.H., Lee, J.H., Lee, J.S., Park, S.O., Lee, S.J., Shin, H.M., Lee, O.H. (2015). The antioxidant activity and their major antioxidant compounds from Acanthopanax senticosus and A. koreanum. Molecules, 20, 13281–13295.
Kimura, Y., Sumiyoshi, M. (2004). Effects of various Eleutherococcus senticosus cortex on swimming time, natural killer activity and corticosterone level in forced swimming stressed mice. J. Ethnopharmacol., 95, 447–453.
Kohlmünzer, S. (2012). Farmakognozja, 5th ed., Wyd. Lek. PZWL, Warsaw, Poland.
Kolesnikov, M.P., Gins, V.K. (2001). Phenolic substances in medicinal plants. Appl. Biochem. Microbiol., 37, 457–465
Kurkin, V.A., Dubishchev, A.V., Ezhkov, V.N., Titova, I.N., Avdeeva, E.V. (2006). Antidepresant activity of some phytopharmaceuticals and phenylpropanoids. Pharm. Chem. J., 40, 33–38.
Lee, H.I., Leon, J., Raskin, I. (1995). Biosynthesis and metabolism of salicylic acid. Proc. Natl. Acad. Sci. U.S.A., 92, 4076–4079.
Liu, S.P., An, J.T., Wang, R., Li, Q. (2012). Simultaneous quantification of five bioactive components of Acanthopanax senticosus and its extract by ultra performance liquid chromatography with electrospray ionization time-of-flight mass spectrometry. Molecules, 17, 7903–7913.
Marrassini, C., Anesini, C., Ferraro, G. (2011). HPLC fingerprint of a flower extract of Tilia × viridis and cor-relation with antiproliferative and antioxidant activity. Phytoter. Res., 25, 1466–1471.
Muñoz-Muñoz, J.L., Garcia-Molina, F., Ros, E., Tudela, J., García-Canovas, F., Rodriguez-Lopez, J.N. (2013). Prooxidant and antioxidant activities of rosmarinic acid. J. Food Biochem., 37, 396–408.
Nishibe, S., Kinoshita, H., Takeda, H., Okano, G. (1990). Phenolic compounds from stem bark of Acanthopanax senticosus and their pharmacological effect in chronic swimming stressed rats. Chem. Pharm. Bull., 38(6), 1763–1765.
Niu, H.S., Liu, I.M., Cheng, J.T., Lin, C.L., Hsu, F.L. (2008). Hypoglycemic effect of syringin from Eleutherococcus senticosus in streptozotocin-induced diabetic rats. Planta Med., 74, 109–113.
Panossian, A., Wikman, G., Wagner, H. (1999). Plant adaptogens III. Earlier and more recent aspects and concepts on their mode of action. Phytomedicine, 6, 287–300.
Rogala, E., Skopińska-Różewska, E., Sawicka, T., Som-mer, E., Prosińska, J., Drozd, J. (2003). The influence of Eleutherococcus senticosus on cellular and humoral immunological response of mice. Pol. J. Vet. Sci., 6(3), 37–39.
Sato, Y., Itagaki, S., Kurokawa, T., Ogura, J., Kobayashi, M., Hirano, T., Sugawara, M., Iseki, K. (2011). In vitro and in vivo antioxidant properties of chlorogenic acid and caffeic acid. Int. J. Pharm., 403, 136–138.
Sevgi, K., Tepe, B., Sarikurkcu, C. (2014). Antioxidant and DNA damage protection potentials of selected phenolic acids. Food Chem. Toxicol., 77, 12–21.
Skiba, A., Węglarz, Z. (1999). Accumulation of biomass and some polyphenolic compounds in Rhaponthicum carthamoides (Willd.) Iljin. Ann. Wars. Agric. Univ. – SGGW, Hortic. Landsc. Archit., 20, 19–25.
Song, Y.Y., Li, Y., Zhang, H.Q. (2010). Therapeutic effect of syringin on adjuvant arthritis in rats and its mechanisms. Acta Pharm. Sin., 45, 1006–1011.
Sytar, O. (2015). Phenolic acids in the inflorescences of different varieties of buckwheat and their antioxidant activity. J. King Saud Univ., 27, 136–142.
Tumiłowicz, J., Banaszczak, P. (2006). Woody species of Araliaceae at the Rogów Arboretum. Rocz. Dendrol., 54, 35–50.
Węglarz, Z., Przybył, J.L., Geszprych, A. (2008). Roseroot (Rhodiola rosea L.): Effect of Internal and External Factors on Accumulation of Biologically Active Com-pounds. Chapter 16. In: Bioactive molecules and medicinal plants, Ramawat, K.G., Mérillon, J.M., (eds.), Springer-Verlag, Berlin-Heidelberg.
Weng, J.K., Chapple, C. (2010). The origin and evolution of lignin biosynthesis. New Phytol., 187, 273–285.
Wu, L., Guo, X., Harivandi, M.A. (1998). Allelopathic effects of phenolic acids detected in buffalograss (Buchloe dactyloides) clippings on growth of annual bluegrass (Poa annua) and buffalograss seedlings. Environ. Exp. Bot., 39, 159–167.
Yazaki, K. (2005). Transporters of secondary metabolites. Curr. Opin. Plant Biol., 8, 301–307.
Yazaki, K. (2006). ABC transporters involved in the transport of plant secondary metabolites. FEBS Lett., 580, 1183–1191.
Yazaki, K., Sugiyama, A., Morita, M., Shitan, N. (2008). Secondary transport as an efficient membrane transport mechanism for plant secondary metabolites. Phyto-chem. Rev., 7, 513–524.
Yilmaz, V.A., Brandolini, A., Hidalgo, A. (2015). Phenolic acids and antioxidant activity of wild, feral and domesticated diploid wheats. J. Cereal Sci., 64, 168–175.
Zhang, T.T, Zheng, C.Y, Hu, W., Xu, W.W., Wang, H.F. (2010). The allelopathy and allelopathic mechanism of phenolic acids on toxic Microcystis aeruginosa. J. Appl. Phycol., 22, 71–77.
Ahn, J., Um, M.Y., Lee, H., Jung, C.H., Heo, S.H., Ha, T.Y. (2013). Eleutheroside E, an active component of Eleutherococcus senticosus, ameliorates insulin resistance in Type 2 diabetic db/db Mice. Evid. Based Complement. Alternat. Med., ID: 934183.
Bakota, E.L., Winkler-Moser, J.K., Berhow, M.A., Eller, F.J., Vaughn, S.F. (2015). Antioxidant activity and sen-sory evaluation of a rosmarinic acid-enriched extract of Salvia officinalis. J. Food Sci., 80, C711–C717.
Bączek, K. (2009). Accumulation of biologically active compounds in Eleuthero (Eleutherococcus senticosus /Rupr. et Maxim./ Maxim.) grown in Poland. Herba Pol., 55, 7–12.
Bączek, K., Banaszczak, P., Przybył, J.L., Węglarz, Z., Pelc, M. (2010). Charakterystyka chemiczna organów nadziemnych i podziemnych 8 gatunków z rodzaju Eleutheroccocus. Zesz. Probl. Post. Nauk. Rol., 555, 163–168.
Bączek, K., Węglarz, Z., Przybył, J.L. (2011). Accumulation of biologically active compounds in the rhizomes and roots of Eleuthero (Eleutherococcus senti-cosus/Maxim. et Rupr./ Maxim.). Adv. Environ. Biol., 5, 325–328.
Chen, M., Song, F., Guo, M., Liu, Z., Liu, S. (2002). Analysis of flavonoid constituents from leaves of Acanthopanax senticosus harms by electrospray tandem mass spectrometry. Rapid Commun. Mass Spectrom., 16(4), 264–271.
Court, W.E. (2000). Ginseng: The Genus Panax. Harwood Academic Publishers, Amsterdam.
Davydov, M., Krikorian, A.D. (2000). Eleutherococcus senticosus (Rupr. & Maxim.) Maxim. (Araliaceae) as an adaptogen: a closer look. J. Ethnopharmacol., 72, 345–393.
Deyama, T., Nishibe, S., Nakazawa, Y. (2001). Constituents and pharmacological effects of Eucommia and Siberian ginseng. Acta Pharmacol. Sin., 22, 1057–1070.
EMA (European Medicines Agency) (2014). Assessment report on Eleutherococcus senticosus (Rupr.et Maxim.) Maxim., radix EMA/HMPC/680615/2013.
Erlejman, A.G., Verstraeten, S.V., Fraga, C.G., Oteiza, P.I. (2004). The interaction of flavonoids with membranes: potential determinant of flavonoid antioxidant effects. Free Radic. Res., 38(12), 1311–1320.
European Pharmacopoeia, 8th ed. (2014). Eleuthero roots – Eleutherococcus radix. European Directorate for the Quality of Medicines and Health Care (EDQM). Council of Europe, Strasbourg, France.
Falé, P.L., Borges, C., Madeira, P.J.A., Ascensão, L., Araújo, M.E.M, Florêncio, M.H, Serralheiro, M.L.M. (2009). Rosmarinic acid, scutellarein 40-methyl ether 7-O-glucuronide and (16S)-coleon E are the main compounds responsible for the antiacetylcholinesterase and antioxidant activity in herbal tea of Plectranthus barbatus („falso boldo”). Food Chem., 114, 798–805.
Glazener, J.A. (1982). Accumulation of phenolic compounds in cells and formation of lignin-like polymers in cell walls of young tomato fruits after inoculation with Botrytis cinerea. Physiol. Plant Pathol., 20, 11–25.
Gong, X., Zhang, L., Jiang, R., Wang, C.D., Yin, X.R., Wan, J.Y. (2013). Hepatoprotective effects of syringin on fulminant hepatic failure induced by D-galactosamine and lipopolysaccharide in mice. J. Appl. Toxicol., 34, 265–271.
Gűlçin, I. (2006). Antioxidant activity of caffeic acid (3,4-dihydroxycinnamic acid). Toxicol., 217, 213–220.
Huang, L.Z., Wei, L., Zhao, H.F., Huang, B.K., Rahman, K., Qin, L.P. (2011). The effect of Eleutheroside E on behavioral alterations in murine sleep deprivation stress model. Eur. J. Pharmacol., 658, 150–155.
Inderjit, S., Streibig, J.C., Olofsdotter, M. (2002). Joint action of phenolic acid mixtures and its significance in allelopathy research. Physiol. Plant., 114, 422–428.
Kakkar, S., Bais, S.A. (2014). Review on protocatechuic acid and its pharmacological potential. ISRN Pharmacol., ID: 952943.
Kim, C.H., Sun, B.Y. (2004). Infrageneric classification of the genus Eleutherococcus Maxim. (Araliaceae) with a new section Cissiflolius. J. Plant Biol., 47, 282–288.
Kim, Y.H., Bae, D.B., Lee, J.S., Park, S.O., Lee, S.J., Cho, O.H., Lee, O.H. (2013). Determination of eleuthero-sides and β-glucan content from different parts and cultivating areas of A. senticosus and A. koreanum. J. Korean Soc. Food Sci. Nutr., 42, 2082–2087.
Kim, Y.H., Cho, M.L., Kim, D., Shin, G.H., Lee, J.H., Lee, J.S., Park, S.O., Lee, S.J., Shin, H.M., Lee, O.H. (2015). The antioxidant activity and their major antioxidant compounds from Acanthopanax senticosus and A. koreanum. Molecules, 20, 13281–13295.
Kimura, Y., Sumiyoshi, M. (2004). Effects of various Eleutherococcus senticosus cortex on swimming time, natural killer activity and corticosterone level in forced swimming stressed mice. J. Ethnopharmacol., 95, 447–453.
Kohlmünzer, S. (2012). Farmakognozja, 5th ed., Wyd. Lek. PZWL, Warsaw, Poland.
Kolesnikov, M.P., Gins, V.K. (2001). Phenolic substances in medicinal plants. Appl. Biochem. Microbiol., 37, 457–465
Kurkin, V.A., Dubishchev, A.V., Ezhkov, V.N., Titova, I.N., Avdeeva, E.V. (2006). Antidepresant activity of some phytopharmaceuticals and phenylpropanoids. Pharm. Chem. J., 40, 33–38.
Lee, H.I., Leon, J., Raskin, I. (1995). Biosynthesis and metabolism of salicylic acid. Proc. Natl. Acad. Sci. U.S.A., 92, 4076–4079.
Liu, S.P., An, J.T., Wang, R., Li, Q. (2012). Simultaneous quantification of five bioactive components of Acanthopanax senticosus and its extract by ultra performance liquid chromatography with electrospray ionization time-of-flight mass spectrometry. Molecules, 17, 7903–7913.
Marrassini, C., Anesini, C., Ferraro, G. (2011). HPLC fingerprint of a flower extract of Tilia × viridis and cor-relation with antiproliferative and antioxidant activity. Phytoter. Res., 25, 1466–1471.
Muñoz-Muñoz, J.L., Garcia-Molina, F., Ros, E., Tudela, J., García-Canovas, F., Rodriguez-Lopez, J.N. (2013). Prooxidant and antioxidant activities of rosmarinic acid. J. Food Biochem., 37, 396–408.
Nishibe, S., Kinoshita, H., Takeda, H., Okano, G. (1990). Phenolic compounds from stem bark of Acanthopanax senticosus and their pharmacological effect in chronic swimming stressed rats. Chem. Pharm. Bull., 38(6), 1763–1765.
Niu, H.S., Liu, I.M., Cheng, J.T., Lin, C.L., Hsu, F.L. (2008). Hypoglycemic effect of syringin from Eleutherococcus senticosus in streptozotocin-induced diabetic rats. Planta Med., 74, 109–113.
Panossian, A., Wikman, G., Wagner, H. (1999). Plant adaptogens III. Earlier and more recent aspects and concepts on their mode of action. Phytomedicine, 6, 287–300.
Rogala, E., Skopińska-Różewska, E., Sawicka, T., Som-mer, E., Prosińska, J., Drozd, J. (2003). The influence of Eleutherococcus senticosus on cellular and humoral immunological response of mice. Pol. J. Vet. Sci., 6(3), 37–39.
Sato, Y., Itagaki, S., Kurokawa, T., Ogura, J., Kobayashi, M., Hirano, T., Sugawara, M., Iseki, K. (2011). In vitro and in vivo antioxidant properties of chlorogenic acid and caffeic acid. Int. J. Pharm., 403, 136–138.
Sevgi, K., Tepe, B., Sarikurkcu, C. (2014). Antioxidant and DNA damage protection potentials of selected phenolic acids. Food Chem. Toxicol., 77, 12–21.
Skiba, A., Węglarz, Z. (1999). Accumulation of biomass and some polyphenolic compounds in Rhaponthicum carthamoides (Willd.) Iljin. Ann. Wars. Agric. Univ. – SGGW, Hortic. Landsc. Archit., 20, 19–25.
Song, Y.Y., Li, Y., Zhang, H.Q. (2010). Therapeutic effect of syringin on adjuvant arthritis in rats and its mechanisms. Acta Pharm. Sin., 45, 1006–1011.
Sytar, O. (2015). Phenolic acids in the inflorescences of different varieties of buckwheat and their antioxidant activity. J. King Saud Univ., 27, 136–142.
Tumiłowicz, J., Banaszczak, P. (2006). Woody species of Araliaceae at the Rogów Arboretum. Rocz. Dendrol., 54, 35–50.
Węglarz, Z., Przybył, J.L., Geszprych, A. (2008). Roseroot (Rhodiola rosea L.): Effect of Internal and External Factors on Accumulation of Biologically Active Com-pounds. Chapter 16. In: Bioactive molecules and medicinal plants, Ramawat, K.G., Mérillon, J.M., (eds.), Springer-Verlag, Berlin-Heidelberg.
Weng, J.K., Chapple, C. (2010). The origin and evolution of lignin biosynthesis. New Phytol., 187, 273–285.
Wu, L., Guo, X., Harivandi, M.A. (1998). Allelopathic effects of phenolic acids detected in buffalograss (Buchloe dactyloides) clippings on growth of annual bluegrass (Poa annua) and buffalograss seedlings. Environ. Exp. Bot., 39, 159–167.
Yazaki, K. (2005). Transporters of secondary metabolites. Curr. Opin. Plant Biol., 8, 301–307.
Yazaki, K. (2006). ABC transporters involved in the transport of plant secondary metabolites. FEBS Lett., 580, 1183–1191.
Yazaki, K., Sugiyama, A., Morita, M., Shitan, N. (2008). Secondary transport as an efficient membrane transport mechanism for plant secondary metabolites. Phyto-chem. Rev., 7, 513–524.
Yilmaz, V.A., Brandolini, A., Hidalgo, A. (2015). Phenolic acids and antioxidant activity of wild, feral and domesticated diploid wheats. J. Cereal Sci., 64, 168–175.
Zhang, T.T, Zheng, C.Y, Hu, W., Xu, W.W., Wang, H.F. (2010). The allelopathy and allelopathic mechanism of phenolic acids on toxic Microcystis aeruginosa. J. Appl. Phycol., 22, 71–77.
Katarzyna Bączek
Warsaw University of Life Science – SGGW, Department of Vegetable and Medicinal Plants, Nowoursynowska 166, 02-787 Warsaw, Poland
Warsaw University of Life Science – SGGW, Department of Vegetable and Medicinal Plants, Nowoursynowska 166, 02-787 Warsaw, Poland
Jarosław L. Przybył
Warsaw University of Life Science – SGGW, Department of Vegetable and Medicinal Plants, Nowoursynowska 166, 02-787 Warsaw, Poland
Warsaw University of Life Science – SGGW, Department of Vegetable and Medicinal Plants, Nowoursynowska 166, 02-787 Warsaw, Poland
Olga Kosakowska
Warsaw University of Life Science – SGGW, Department of Vegetable and Medicinal Plants, Nowoursynowska 166, 02-787 Warsaw, Poland
Warsaw University of Life Science – SGGW, Department of Vegetable and Medicinal Plants, Nowoursynowska 166, 02-787 Warsaw, Poland
Zenon Węglarz
Warsaw University of Life Science – SGGW, Department of Vegetable and Medicinal Plants, Nowoursynowska 166, 02-787 Warsaw, Poland
Warsaw University of Life Science – SGGW, Department of Vegetable and Medicinal Plants, Nowoursynowska 166, 02-787 Warsaw, Poland
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