Plant-growth regulators alter phytochemical constituents and pharmaceutical quality in Sweet potato (Ipomoea batatas L.)
Tóm tắt
Sweet potato (Ipomoea batatas L.) is one of the most important consumed crops in many parts of the world because of its economic importance and content of health-promoting phytochemicals. With the sweet potato (Ipomoea batatas L.) as our model, we investigated the exogenous effects of three plant-growth regulators methyl jasmonate (MeJA), salicylic acid (SA), and abscisic acid (ABA) on major phytochemicals in relation to phenylalanine ammonia lyase (PAL) activity. Specifically, we investigated the total phenolic content (TPC), total flavonoid content (TFC), total anthocyanin content (TAC), and total β-carotene content (TCC). Individual phenolic and flavonoid compounds were identified using ultra-high performance liquid chromatography (UHPLC). Antioxidant activities of treated plants were evaluated using a 1,1-diphenyl-2-picrylhydrazyl (DPPH) assay and a β-carotene bleaching assay. Anticancer activity of extracts was evaluated against breast cancer cell lines (MCF-7 and MDA-MB-231) using MTT assay. TPC, TFC, TAC, and TCC and antioxidant activities were substantially increased in MeJA-, SA-, and ABA-treated plants. Among the secondary metabolites identified in this study, MeJA application significantly induced production of quercetin, kaempferol, myricetin, gallic acid, chlorogenic acid, 3,5-dicaffeoylquinic acid, and 4,5-dicaffeoylquinic acid. Luteolin synthesis was significantly induced by SA application. Compared with control plants, MeJA-treated sweet potato exhibited the highest PAL activity, followed by SA and ABA treatment. The high DPPH activity was observed in MeJA followed by SA and ABA, with half-maximal inhibitory concentration (IC50) values of 2.40, 3.0, and 3.40 mg/mL compared with α-tocopherol (1.1 mg/mL). Additionally, MeJA-treated sweet potato showed the highest β-carotene bleaching activity, with an IC50 value of 2.90 mg/mL, followed by SA (3.30 mg/mL), ABA (3.70 mg/mL), and control plants (4.5 mg/mL). Extracts of sweet potato root treated with MeJA exhibited potent anticancer activity with IC50 of 0.66 and 0.62 mg/mL against MDA-MB-231 and MCF-7 cell lines respectively, compared to that of extracts of sweet potato treated with SA (MDA-MB-231 = 0.78 mg/mL; MCF-7 = 0.90 mg/mL) and ABA (MDA-MB-231 = 0.94 mg/mL; MCF-7 = 1.40 mg/mL). The results of correlation analysis showed that anthocyanins and flavooids are corresponding compounds in sweet potato root extracts for anticancer activity against breast cancer cell lines. MeJA has great potential to enhance the production of important health-promoting phytochemicals in sweet potato.
Tài liệu tham khảo
Bovell‐Benjamin AC. Sweet potato: a review of its past, present, and future role in human nutrition. Adv Food Nutr Res. 2007;52:1–59.
Cho J, Kang JS, Long PH, Jing J, Back Y, Chung K-S. Antioxidant and memory enhancing effects of purple sweet potato anthocyanin and cordyceps mushroom extract. Arch Pharm Res. 2003;26(10):821–5.
Teow CC, Truong V-D, McFeeters RF, Thompson RL, Pecota KV, Yencho GC. Antioxidant activities, phenolic and β-carotene contents of sweet potato genotypes with varying flesh colours. Food Chem. 2007;103(3):829–38.
Karna P, Gundala SR, Gupta MV, Shamsi SA, Pace RD, Yates C, Narayan S, Aneja R. Polyphenol-rich sweet potato greens extract inhibits proliferation and induces apoptosis in prostate cancer cells in vitro and in vivo. Carcinogenesis. 2011;32(12):1872-80. doi:10.1093/carcin/bgr215.
Kusano S, Abe H. Antidiabetic activity of white skinned sweet potato (Ipomoea batatas L.) in obese Zucker fatty rats. Biol Pharm Bull. 2000;23(1):23–6.
Zhang Z-F, Fan S-H, Zheng Y-L, Lu J, Wu D-M, Shan Q, Hu B. Purple sweet potato color attenuates oxidative stress and inflammatory response induced by D-galactose in mouse liver. Food Chem Toxicol. 2009;47(2):496–501.
Van den Berg H, Faulks R, Granado HF, Hirschberg J, Olmedilla B, Sandmann G, Southon S, Stahl W. The potential for the improvement of carotenoid levels in foods and the likely systemic effects. J Sci Food Agric. 2000;80(7):880–912.
Truong VD, McFeeters R, Thompson R, Dean L, Shofran B. Phenolic acid content and composition in leaves and roots of common commercial sweet potato (Ipomea batatas L.) cultivars in the United States. J Food Sci. 2007;72(6):C343–9.
Padda MS, Picha DH. Quantification of phenolic acids and antioxidant activity in sweet potato genotypes. Sci Hortic. 2008;119(1):17–20.
Ren W, Qiao Z, Wang H, Zhu L, Zhang L. Flavonoids: promising anticancer agents. Med Res Rev. 2003;23(4):519–34.
Ghasemzadeh A, Ghasemzadeh N. Flavonoids and phenolic acids: Role and biochemical activity in plants and human. J Med Plants Res. 2011;5(31):6697–703.
Gomes CA, Girão da Cruz T, Andrade JL, Milhazes N, Borges F, Marques MPM. Anticancer activity of phenolic acids of natural or synthetic origin: a structure-activity study. J Med Chem. 2003;46(25):5395–401.
Bari R, Jones JD. Role of plant hormones in plant defence responses. Plant Mol Biol. 2009;69(4):473–88.
Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol. 2006;9(4):436–42.
Horváth E, Szalai G, Janda T. Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul. 2007;26(3):290–300.
Ghasemzadeh A, Jaafar HZ. Effect of salicylic acid application on biochemical changes in ginger (Zingiber officinale Roscoe). J Med Plants Res. 2012;6(5):790–5.
Ghasemzadeh A, Jaafar HZ, Karimi E. Involvement of salicylic acid on antioxidant and anticancer properties, anthocyanin production and chalcone synthase activity in ginger (Zingiber officinale Roscoe) varieties. Int J Mol Sci. 2012;13(11):14828–44.
Zhang W, Curtin C, Kikuchi M, Franco C. Integration of jasmonic acid and light irradiation for enhancement of anthocyanin biosynthesis in Vitis vinifera suspension cultures. Plant Sci. 2002;162(3):459–68.
Li Z, Zhao X, Sandhu AK, Gu L. Effects of exogenous abscisic acid on yield, antioxidant capacities, and phytochemical contents of greenhouse grown lettuces. J Agric Food Chem. 2010;58(10):6503–9.
MacDonald MJ, D’Cunha GB. A modern view of phenylalanine ammonia lyase. Biochem Cell Biol. 2007;85(3):273–82.
Koes RE, Quattrocchio F, Mol JN. The flavonoid biosynthetic pathway in plants: function and evolution. BioEssays. 1994;16(2):123–32.
Lister CE, Lancaster JE, Walker JR. Phenylalanine ammonia-lyase (PAL) activity and its relationship to anthocyanin and flavonoid levels in New Zealand-grown apple cultivars. J Am Soc Horticult Sci. 1996;121(2):281–5.
Aydas SB, Ozturk S, Aslim B. Phenylalanine ammonia lyase (PAL) enzyme activity and antioxidant properties of some cyanobacteria isolates. Food Chem. 2013;136(1):164–9.
Jiang Y, Joyce DC. ABA effects on ethylene production, PAL activity, anthocyanin and phenolic contents of strawberry fruit. Plant Growth Regul. 2003;39(2):171–4.
Koca N, Karaman Ş. The effects of plant growth regulators and l-phenylalanine on phenolic compounds of sweet basil. Food Chem. 2015;166:515–21.
Nakatani M, Koda Y. Identification of jasmonic acid and its effects on root development in sweet potato, Low-input Sustainable Crop Production Systems in Asia, KSCS, Korea. 1993. p. 523–31.
Wojdyło A, Oszmiański J, Czemerys R. Antioxidant activity and phenolic compounds in 32 selected herbs. Food Chem. 2007;105(3):940–9.
Cheng GW, Breen PJ. Activity of phenylalanine ammonia-lyase (PAL) and concentrations of anthocyanins and phenolics in developing strawberry fruit. J Am Soc Horticult Sci. 1991;116(5):865–9.
Sun B, Yan H, Zhang F, Wang Q. Effects of plant hormones on main health-promoting compounds and antioxidant capacity of Chinese kale. Food Res Int. 2012;48(2):359–66.
Kim H-J, Fonseca JM, Choi J-H, Kubota C. Effect of methyl jasmonate on phenolic compounds and carotenoids of romaine lettuce (Lactuca sativa L.). J Agric Food Chem. 2007;55(25):10366–72.
Ali MB, Hahn E-J, Paek K-Y. Methyl jasmonate and salicylic acid induced oxidative stress and accumulation of phenolics in Panax ginseng bioreactor root suspension cultures. Molecules. 2007;12(3):607–21.
Kano M, Takayanagi T, Harada K, Makino K, Ishikawa F. Antioxidative activity of anthocyanins from purple sweet potato, Ipomoera batatas cultivar Ayamurasaki. Biosci Biotechnol Biochem. 2005;69(5):979–88.
Shan X, Zhang Y, Peng W, Wang Z, Xie D. Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis. J Exp Bot. 2009;60(13):3849–60.
Saniewski M, Horbowicz M, Puchalski J, Ueda J. Methyl jasmonate stimulates the formation and the accumulation of anthocyanin in Kalanchoe blossfeldiana. Acta Physiol Plant. 2003;25(2):143–9.
Ghasemzadeh A, Jaafar HZ, Karimi E, Ibrahim MH. Combined effect of CO2 enrichment and foliar application of salicylic acid on the production and antioxidant activities of anthocyanin, flavonoids and isoflavonoids from ginger. BMC Complement Altern Med. 2012;12(1):1.
Barickman TC, Kopsell DA, Sams CE. Abscisic acid increases carotenoid and chlorophyll concentrations in leaves and fruit of two tomato genotypes. J Am Soc Horticult Sci. 2014;139(3):261–6.
Steed L, Truong VD. Anthocyanin content, antioxidant activity, and selected physical properties of flowable purple‐fleshed sweet potato purees. J Food Sci. 2008;73(5):S215–21.
Cevallos-Casals BA, Cisneros-Zevallos L. Stability of anthocyanin-based aqueous extracts of Andean purple corn and red-fleshed sweet potato compared to synthetic and natural colorants. Food Chem. 2004;86(1):69–77.
Oki T, Masuda M, Furuta S, Nishiba Y, Terahara N, Suda I. Involvement of anthocyanins and other phenolic compounds in radical scavenging activity of purple fleshed sweet potato cultivars. J Food Sci. 2002;67(5):1752–6.
Bahorun T, Luximon‐Ramma A, Crozier A, Aruoma OI. Total phenol, flavonoid, proanthocyanidin and vitamin C levels and antioxidant activities of Mauritian vegetables. J Sci Food Agric. 2004;84(12):1553–61.
Dixon RA, Paiva NL. Stress-induced phenylpropanoid metabolism. Plant Cell. 1995;7(7):1085.
Sun Z, Hou S, Yang W, Han Y. Exogenous application of salicylic acid enhanced the rutin accumulation and influenced the expression patterns of rutin biosynthesis related genes in Fagopyrum tartaricum Gaertn leaves. Plant Growth Regul. 2012;68(1):9–15.
de la Peña Moreno F, Blanch GP, del Castillo ML R. (+)-Methyl jasmonate-induced bioformation of myricetin, quercetin and kaempferol in red raspberries. J Agric Food Chem. 2010;58(22):11639–44.
Ku KM, Juvik JA. Environmental stress and methyl jasmonate-mediated changes in flavonoid concentrations and antioxidant activity in broccoli florets and kale leaf tissues. Hortscience. 2013;48(8):996–1002.
Hung KT, Kao CH. Hydrogen peroxide is necessary for abscisic acid-induced senescence of rice leaves. J Plant Physiol. 2004;161(12):1347–57.
Montero T, Mollá E, Mart Cabrejas MA, Là pez Andru FJ. Effects of gibberellic acid (GA3) on strawberry PAL (phenylalanine ammonia-lyase) and TAL (tyrosine ammonia-lyase) enzyme activities. J Sci Food Agric. 1998;77(2):230–4.
Huang D-J, Chun-Der L, Hsien-Jung C, Yaw-Huei L. Antioxidant and antiproliferative activities of sweet potato (Ipomoea batatas [L.] LamTainong 57’) constituents. Bot Bull Acad Sin. 2004;45:179-86.
Huang Y-C, Chang Y-H, Shao Y-Y. Effects of genotype and treatment on the antioxidant activity of sweet potato in Taiwan. Food Chem. 2006;98(3):529–38.
Rumbaoa RGO, Cornago DF, Geronimo IM. Phenolic content and antioxidant capacity of Philippine sweet potato (Ipomoea batatas) varieties. Food Chem. 2009;113(4):1133–8.
Ghasemzadeh A, Jaafar HZ, Rahmat A, Ashkani S. Secondary metabolites constituents and antioxidant, anticancer and antibacterial activities of Etlingera elatior (Jack) RM Sm grown in different locations of Malaysia. BMC Complement Altern Med. 2015;15(1):335
Ghasemzadeh A, Jaafar HZ. Profiling of phenolic compounds and their antioxidant and anticancer activities in pandan (Pandanus amaryllifolius Roxb.) extracts from different locations of Malaysia. BMC Complement Altern Med. 2013;13(1):341.
Kumazawa S, Taniguchi M, Suzuki Y, Shimura M, Kwon M-S, Nakayama T. Antioxidant activity of polyphenols in carob pods. J Agric Food Chem. 2002;50(2):373–7.
Sakanaka S, Tachibana Y, Okada Y. Preparation and antioxidant properties of extracts of Japanese persimmon leaf tea (kakinoha-cha). Food Chem. 2005;89(4):569–75.
Agarwal S, Sairam R, Srivastava G, Meena R. Changes in antioxidant enzymes activity and oxidative stress by abscisic acid and salicylic acid in wheat genotypes. Biol Plant. 2005;49(4):541–50.
Ghasemzadeh A, Jaafar HZ. Interactive effect of salicylic acid on some physiological features and antioxidant enzymes activity in ginger (Zingiber officinale Roscoe). Molecules. 2013;18(5):5965–79.
Itharat A, Houghton PJ, Eno-Amooquaye E, Burke P, Sampson JH, Raman A. In vitro cytotoxic activity of Thai medicinal plants used traditionally to treat cancer. J Ethnopharmacol. 2004;90(1):33–8.
Sugata M, Lin C-Y, Shih Y-C. Anti-Inflammatory and Anticancer Activities of Taiwanese Purple-Fleshed Sweet Potatoes (Ipomoea batatas L. Lam) Extracts. BioMed Res Int. 2015;2015:10. http://www.hindawi.com/journals/bmri/2015/768093/abs/.
Li P-G, Mu T-H, Deng L. Anticancer effects of sweet potato protein on human colorectal cancer cells. World J Gastroenterol. 2013;19(21):3300.
Nile SH, Park SW. Edible berries: Bioactive components and their effect on human health. Nutrition. 2014;30(2):134–44.
Li W-Y, Chan S-W, Guo D-J, Yu PH-F. Correlation between antioxidative power and anticancer activity in herbs from traditional Chinese medicine formulae with anticancer therapeutic effect. Pharm Biol. 2007;45(7):541–6.
Heim KE, Tagliaferro AR, Bobilya DJ. Flavonoid antioxidants: chemistry, metabolism and structure-activity relationships. J Nutr Biochem. 2002;13(10):572–84.