All Issue

2018 Vol.31, Issue 4 Preview Page
August 2018. pp. 342-354
Abstract

Suaeda japonica is a halophytic plant that lives in mudflat at intertidal zone of western and southern coastal areas of Korea. The seawater-living plants showed a purple color during their whole life. In contrast, freshwater-living plants displayed a green color in leaves. When seawater-living plants were transferred to potting soil, the purple color was gradually changed to green in the leaves. The extracted purple pigment compound exhibited typical characteristics of betacyanin that were represented by water solubility, pH- and temperature-dependent color changes, sensitivity to light, UV-Vis spectra, and gel electrophoretic migration pattern. The LC-MS analysis of the extracted pigment compound showed the presence of two major protonated molecular ions ([M+H]+) at m/z 651.1 and m/z 827.1. Antioxidant activity of the pigment compound was determined using stable free radical DPPH assay. It was found to have an antioxidant activity that is linearly increased in proportion to the reaction time for up to 30 min, and the activity was comparable to that of control BHA at 9.0 ㎎/㎖. The anticancer activity against several tumor cell lines was also examined following the MTT assay. The significant growth inhibitory effect was observed on two tumor cell lines, SW-156 (human kidney carcinoma) and HEC-1B (human endometrial adenocarcinoma). Probably, the pigment compound may function as an osmolyte to uphold halotolerant physiological processes in saline environment.

References
  1. Adams, P., D. Nelson, S. Yamada, W. Chmara, R.G. Jensrn, H.J. Bohnert and H. Griffiths. 1998. Growth and development of Mesembryanthemum crystallinum (Aizoaceae). New Phytol. 138:171-190.10.1046/j.1469-8137.1998.00111.x
  2. Alhdad, G.M., C.E. Seal, M.J. Al-Azzawi and T.J. Flowers. 2013. The effect of combined salinity and waterlogging on the halophyte Suaeda maritima: The role of antioxidants. Environ. Exp. Bot. 87:120-125.10.1016/j.envexpbot.2012.10.010
  3. Allegra, M., P.G. Furtmüller, W. Jantschko, M. Zederbauer, L. Tesoriere, M. Livrea and C. Obinger. 2005. Mechanism of interaction of betanin and indicaxanthin with human myeloperoxidase and hypochlorous acid. Biochem. Biophys. Res. Comm. 332:837-844. 10.1016/j.bbrc.2005.05.03115913556
  4. Ayarpadikannan, S., E.S., Chung, C.W. Cho, H.A. So, S.O. Kim, J.M. Jeon, M.H. Kwak, S.W. Lee and J.H. Lee. 2012. Exploration for the salt stress tolerance genes from a salt- treated halophyte, Suaeda asparagoides. Plant Cell Rep. 31:35-48.10.1007/s00299-011-1137-421874516
  5. Betancourt, C., M.J. Cejudo-Bastante, F.J. Heredia and N. Hurtado. 2017. Pigment composition and antioxidant capacity of betacyanins and betaxanthins fractions of Opuntia dillenii (Ker Gawl) haw cactus fruit. Food Res. Int. 101:173-179. 10.1016/j.foodres.2017.09.00728941681
  6. Barbour, M.G. and G. Michael. 1970. Is any angiosperm an obligate halophyte?. Amer. Midland Naturalist 84:106-119.10.2307/2423730
  7. Barbour, M.G., J.H. Burk and W.D. Pitts. 1987. Terrestrial Plant Ecology. Second ed, Benjamin/Cummings Pub. Co., Menlo Park, CA (USA). PMC260699
  8. Blois, M.S. 1958. Antioxidant determinations by the use of a stable free radical. Nature 181:1199-2000.10.1038/1811199a0
  9. Bothe, H. 1976. Salzresistenz bei Pflanzen. Biologie in unserer Zeit. 6:3-9. 10.1002/biuz.19760060103
  10. Cabrita, L., T. Fossen and Ø.M. Andersen. 2000. Colour and stability of the six common anthocyanidin 3-glucosides in aqueous solutions. Food Chem. 68:101-107.10.1016/S0308-8146(99)00170-3
  11. Cai, Y., M. Sun and H. Corke. 2001. Identification and distribution of simple and acylated betacyanins in Amaranthacea. J. Agric. Food Chem. 49:1971-1978.10.1021/jf000963h
  12. Cai, Y., M. Sun, H. Wu, R. Huang and H. Corke. 1998. Characterization and quantification of betacyanin pigments from diverse Amaranthus species. J. Agric. Food Chem. 46:2063-2070. 10.1021/jf9709966
  13. Caldas-Cueva, J.P., P. Morales, F. Ludena, I. Betalleluz- Pallardel, R. Chirinos, G. Noratto and D. Campos. 2015. Stability of betacyanin pigments and antioxidants in ayrampo (Opuntia soehrensii Britton and Rose) seed extracts and as a yogurt natural colorant. J. Food Processing & Preservation 40:541-549.10.1111/jfpp.12633
  14. Castellar, R., J.M., Obón, M. Alacid and J.A. Fernández-López. 2003. Color properties and stability of betacynins from Opuntia fruits. J. Agric. Food Chem. 51:2772-2776.10.1021/jf021045h12696971
  15. Chirol, N. and M. Jay. 1995. Acylated anthocyanins from flowers of Begonia. Phytochemistry 40:275-277.10.1016/0031-9422(95)00073-G
  16. Choi, J.H., S.K. Yoon, K.H. Lee, M.S. Seo, D.H. Kim, S.B. Hong, J.Y. Kim, H.D. Paik and C.H. Kim. 2006. Antitumor activity of cell suspension culture of green tea seed (Camellia sinensis L.). Biotechnol. Bioprocess Eng. 11:396-401.10.1007/BF02932305
  17. Chung, S.H. and Y.H. Byun. 2009. Convenient methods for the extraction and discrimination of water-soluble plant pigments. J. Kor. Contents Association 9:353-360.10.5392/JKCA.2009.9.3.353
  18. Flowers, T.J., M.A. Hajibaggheri and N.J.W. Clipson. 1986. Halophytes. Quart. Rev. Biol. 61:313-337.10.1086/415032
  19. Flowers, T.J. and T.D. Colmer. 2008. Salinity tolerance in halophytes. New Phytol. 179:945-963.10.1111/j.1469-8137.2008.02531.x18565144
  20. Flowers, T.J. and T.D. Colmer. 2015. Plant salt tolerance: adaptations in halophytes. Ann. Bot. 115:327-331.10.1093/aob/mcu26725844430PMC4332615
  21. Fossen, T. and Ø.M. Andersen. 1999. Cyanidin 3-(2”,3”- digalloylglucoside) from red leaves of Acer platanoides. Phytochemistry 52:1697-1700. 10.1016/S0031-9422(99)00188-0
  22. Gandía-Herrero, F., F. García-Carmona and J. Escribano. 2005. Fluorescent pigments: new perspectives in betalain research and applications. Food Res. Intl. 38:879-884.10.1016/j.foodres.2005.01.012
  23. Glenn, E.P., J.J. Brown and J.W. O'Leary. 1998. Irrigating crops with seawater. Sci. Amer. August. pp.76-81. 10.1038/scientificamerican0898-76
  24. Goto, T., T. Hoshino and M. Ohba. 1976. Stabilization effect of neutral salts on anthocyanins: flavylium salts, anhydrobases and genuine anthocyanins. Agr. Biol. Chem. 40:1593-1596.10.1271/bbb1961.40.159310.1080/00021369.1976.10862247
  25. Goto, T., T. Kondo, H. Tamura and K. Kawahori. 1983. Structure of platiconin, a diacylated anthocyanin isolated from the Chinese bell-flower Platycodon grandiflorum. Tetrahedron Letters 24:2181-2184.10.1016/S0040-4039(00)81877-8
  26. Hong, S., Lee H.A., Y.S. Lee, D.W. Kim, J.H. Jeonh, T.W. Kim and O. Kim. 2014. Anti-toxoplasmosis effect of the halophyte Suaeda maritima. Korean J. Plant Res. 27:415-420.10.7732/kjpr.2014.27.5.415
  27. Jackman, R.L. and J.L. Smith. 1996. Anthocyanins and betalains: In Hendry G.A.F. and J.D. Houghton (eds.), Natural Food Colorants (2nd ed.), Chapman & Hall, London, UK. pp. 245-309.10.1007/978-1-4615-2155-6_8
  28. Jang, Y.P., J. Zhou, K. Nakanishi and J.R. Sparrow. 2005. Anthocyanins protect against A2E photooxidation and membrane permeabilization in retinal pigment epithelial cells. Photochem. Photobiol. 81:529-536.10.1111/j.1751-1097.2005.tb00221.x10.1562/2004-12-14-RA-402.115745429PMC1351305
  29. Kang, K.Y., Y.H. Hwang, S.J. Lee, J.J. Kim, S.J. Nam and S.T. Yee. 2017. Verification of the antioxidant activity of a subterranean part of Suaeda japonica Makino. Industrial Crops & Products 109:836-842.10.1016/j.indcrop.2017.09.049
  30. Kim, H.R., G.N. Park, B.K. Jung, W.J. Yoon, Y.H. Jung and K.S. Chang. 2016. Antibacterial activity of Suaeda australis in halophyte. J. Kor. Oil Chemist’s Soc. 33:278-285.10.12925/jkocs.2016.33.2.278
  31. Kim, S.D., J.H. Do and H.I. Oh. 1981. Antioxidant activity of Panax ginseng browning products. J. Kor. Agr. Chem. Soc. 24:161-166.
  32. Larcher, W. 1995. Physiological Plant Ecology - Ecophysiology and Stress Physiology of Functional Groups. Third ed, Springer. pp. 396-409.
  33. Lohachoompol, V., M. Mulholland, G. Srzednicki and J. Craske. 2008. Determination of anthocyanins in various cultivars of highbush and rabbit eye blueberries. Food Chem. 111: 249-254.10.1016/j.foodchem.2008.03.067
  34. Nelson, N. and W. Harvey. 1999. Vacuolar and plasma membrane proton adenosinetriphosphatases. Physiol. Rev. 79:361-385.10.1152/physrev.1999.79.2.36110221984
  35. Pollard, A. and R.G. Wyn Jones. 1979. Enzyme activities in concentrated solutions of glycine betaine and other solutes. Planta 144:291-298.10.1007/BF0038877224407261
  36. Rubinstein, L.V., R.H. Shoemaker, K.D. Paull, R.M. Simon, S. Tosini, P. Skehan, D.A. Scudiero, A. Monks and M.R. Boyd. 1990. Comparison of in vitro anticancer-drug-screening data generated with a tetrazolium assay versus a protein assay against a diverse panel of human tumor cell lines. J. Natl. Cancer Inst. 82:1113-1118.10.1093/jnci/82.13.11132359137
  37. Saito, N., F. Tatsuzawa, K. Kasahara, M. Yokoi, S. Iida, A. Shigihara and T. Honda. 1996. Acylated peonidin glycosides in the slate flowers of Pharbitis nil. Phytochemistry 41: 1607-1611.10.1016/0031-9422(95)00822-5
  38. Schliemann, W., R.W. Joy IV, A. Komamine, J.W. Metzger, M. Nimtz, V. Wray and D. Strack. 1996. Betacyanins from plants and cell cultures of Phytolacca americana. Phytochemistry 42:1039-1046.10.1016/0031-9422(96)00100-8
  39. Schliemann, W., Y. Cai, T. Degenkolb, J. Schmidt and H. Corke. 2001. Betalains of Celosia argentea. Phytochemistry 58:159-165.10.1016/S0031-9422(01)00141-8
  40. Song, J. and B.S. Wang. 2015. Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Ann. Bot. 115:541-553.10.1093/aob/mcu19425288631PMC4332605
  41. Stafford, H.A. 1994. Anthocyanins and betalains: evolution of the mutually exclusive pathways. Plant Sci. 101:91-98.10.1016/0168-9452(94)90244-5
  42. Steglich, W. and D. Strack. Betalains. 1990: In Brossi A.A. (ed.), The Alkaloids - Chemistry and Pharmacology, Vol. 39, Academic Press, San Diego, USA. pp. 1-62.
  43. Stintzing F.C. and R. Carle. 2004. Functional properties of anthocyanins and betalanins in plants, food, and in human nutrition. Trends Food Sci. Technol. 15:19-38.10.1016/j.tifs.2003.07.004
  44. Strack, D., T. Vogt and W. Schliemann. 2003. Recent advances in betalain research. Phytochemistry 62:247-269.10.1016/S0031-9422(02)00564-2
  45. Tanaka, Y., N. Sasaki and A. Ohmiya. 2008. Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. The Plant J. 54:733-749.10.1111/j.1365-313X.2008.03447.x18476875
  46. Tsai, P.J., C.H. Sheu, P.H. Wu and Y.F. Sun. 2010. Thermal and pH stability of betacynin pigment of Djulis (Chenopodium formosanum) in Taiwan and their relation to antioxidant activity. J. Agric. Food Chem. 58:1020-1025.10.1021/jf903276620030318
  47. Woo, K.K., F.H. Ngou, L.S., Ngo, W.K. Soong and P.Y. Tang. 2011. Stability of betalain pigment from red dragon fruit (Hylocereus polyrhizus). Amer. J. Food Technol. 6:140-148.10.3923/ajft.2011.140.148
  48. Wyler, H. and A.S. Dreiding. 1961. Über Betacyane, die Stickstoffhaltigen Farbstoffe der Centrospermen - Vorlaufige Mitteilung. Experientia 17:23-25.10.1007/BF0215793113831375
  49. Xu, Y., Y. Zhao, H. Duan, N.S. Fang and J. Song. 2017. Transcriptomic profiling of genes in matured dimorphic seeds of euhalophyte Suaeda salsa. BMC Genomics 18:727-740. 10.1186/s12864-017-4104-928903734PMC5598043
  50. Yang, R.Y.K., O. Bayraktar and H.T. Pu. 2003. Plant-cell bioreactors with simultaneous electropermeabilization and electrophoresis. J. Biotechnol. 100:13-22.10.1016/S0168-1656(02)00226-2
Information
  • Publisher :The Plant Resources Society of Korea
  • Publisher(Ko) :한국자원식물학회
  • Journal Title :Korean Journal of Plant Resources
  • Journal Title(Ko) :한국자원식물학회지
  • Volume : 31
  • No :4
  • Pages :342-354
  • Received Date :2018. 04. 04
  • Accepted Date : 2018. 08. 17