Abstract
Esterification of xanthophylls is important for improving their bioactive potency. The effects of metal cations on esterified xanthophyll biosynthesis and on the accumulation and composition of salt stress-induced carotenoids were investigated in the aerial microalga Coelastrella sp. KGU-Y002 (Chlorophyta, Scenedesmaceae). Under nitrogen-deficient and high-light conditions, salt-supplemented cultures showed enhanced synthesis of esterified astaxanthin, adonixanthin, and zeaxanthin. In particular, KCl supplementation caused a remarkable increase in esterification, such that 73 % of xanthophylls were esterified. After 1 day of KCl treatment, the concentration of endogenous abscisic acid had increased to 200-fold its initial concentration. In algal cells treated with abscisic acid in nitrogen-deficient and high-light conditions, the reactive oxygen species concentration was almost the same as that in the KCl-supplemented culture. In these algal cells, abscisic acid enhanced esterification without affecting total carotenoid accumulation. These findings suggested that xanthophyll esterification is regulated during the response to salt stress by abscisic acid, which has plant hormone-like bioactivity in this aerial microalga. Further studies have been designed to examine large-scale production of esterified xanthophylls by this aerial microalga under salt-stress conditions, and to assess the bioactivity of esterified xanthophylls extracted from algal cells.
Similar content being viewed by others
References
Abe K, Hattori H, Hirano M (2007) Accumulation and antioxidant activity of secondary carotenoids in the aerial microalga Coelastrella striolata var. multistriata. Food Chem 100:656–661
Abe K, Bito T, Sato A, Aburai N (2014) Effects of light intensity and magnesium supplementation in pretreatment cycle on ammonium removal from wastewater of photobioreactor using a biofilter composed of the aerial microalga Trentephohlia aurea. J Appl Phycol 26:341–347
Aburai N, Ohkubo S, Miyashita H, Abe K (2013) Composition of carotenoids and identification of aerial microalgae isolated from the surface of rocks in mountainous districts of Japan. Algal Res 2:237–243
Aburai N, Sumida D, Abe K (2015) Effect of light level and salinity on the composition and accumulation of free and ester-type carotenoids in the aerial microalga Scenedesmus sp. (Chlorophyceae). Algal Res 8:30–36
Chang CCY, Miyazaki A, Dong R, Kheirollah A, Yu C, Geng Y, Higgs HN, Chang TY (2010) Purification of recombinant acyl-coenzyme A: cholesterol acyltransferase 1 (ACAT1) from H293 cells and binding studies between the enzyme and substrates using difference intrinsic fluorescence spectroscopy. Biochemistry 49:9957–9963
Chen G, Wang B, Han D, Sommerfeld M, Lu Y, Chen F, Hu Q (2015) Molecular mechanisms of the coordination between astaxanthin and fatty acid biosynthesis in Haematococcus pluvialis (Chlorophyceae). Plant J 81:95–107
Chu FL, Pirastru L, Popovic R, Sleno L (2011) Carotenogenesis up-regulation in Scenedesmus sp. using a targeted metabolomics approach by liquid chromatography-high-resolution mass spectrometry. J Agric Food Chem 59:3004–3013
Cutler AJ, Krochko JE (1999) Formation and breakdown of ABA. Trends Plant Sci 4:472–478
Gorain PC, Bagchi SK, Mallick N (2013) Effects of calcium, magnesium and sodium chloride in enhancing liquid accumulation in two green microalgae. Environ Technol 34:1887–1894
Goss R, Jakob T (2010) Regulation and function of xanthophyll cycle-dependent photoprotection in algae. Photosynth Res 106:103–122
Hirsch R, Hartung W, Gimmler H (1989) Abscisic acid content of algae under stress. Bot Acta 102:326–334
Hou S, Zhu J, Ding M, Lv G (2008) Simultaneous determination of gibberellic acid, indole-3-acetic acid and abscisic acid in wheat extracts by solid-phase extraction and liquid chromatography-electrospray tandem mass spectrometry. Talanta 76:798–802
Kamath BS, Srikanta BM, Dharmesh SM, Sarada R, Ravishankar GA (2008) Ulcer preventive and antioxidative properties of astaxanthin from Haematococcus pluvialis. Eur J Pharmacol 590:387–395
Kaufnerová V, Eliáš M (2013) The demise of the genus Scotiellopsis Vinatzer (Chlorophyta). Nova Hedwigia 97:415–428
Kobayashi M, Sakamoto Y (1999) Singlet oxygen quenching ability of astaxanthin esters from the green alga Haematococcus pluvialis. Biotechnol Lett 21:265–269
Kobayashi M, Hirai N, Kurimura Y, Ohigashi H, Tsuji Y (1997) Abscisic acid-dependent algal morphogenesis in the unicellular green alga Haematococcus pluvialis. Plant Growth Regul 22:79–85
Maoka T, Yasui H, Ohmori A, Tokuda H, Suzuki N, Osawa A, Shindo K, Ishibashi T (2013) Anti-oxidative, anti-tumor-promoting, and anti-carcinogenic activities of adonirubin and adonixanthin. J Oleo Sci 62:181–186
Mittler R, Blumwald E (2015) The roles of ROS and ABA in systemic acquired acclimation. Plant Cell 27:64–70
Pancha I, Chokshi K, Maurya R, Trivedi K, Patidar SK, Ghosh A, Mishra S (2015) Salinity induced oxidative stress enhanced biofuel production potential of microalgae Scenedesmus sp. CCNM 1077. Bioresour Technol 189:341–348
Rao AR, Sindhuja HN, Dharmesh SM, Sankar KU, Sarada R, Ravishankar GA (2013) Effective inhibition of skin cancer, tyrosinase, and antioxidative properties by astaxanthin and astaxanthin esters from the green alga Haematococcus pluvialis. J Agric Food Chem 61:3842–3851
Rao AR, Sarada R, Shylaja MD, Ravishankar GA (2015) Evaluation of hepatoprotective and antioxidant activity of astaxanthin and astaxanthin esters from microalga-Haematococcus pluvialis. J Food Sci Technol 52:6703–6710
Rosenkranz AR, Schmaldienst S, Stuhlmeier KM, Chen W, Knapp W, Zlabinger GJ (1992) A microplate assay for the detection of oxidative products using 2′, 7′ –dichlorofluorescin-diacetate. J Immunol Methods 156:39–45
Sajilata MG, Singhal RS, Kamat MY (2008) The carotenoid pigment zeaxanthin—a review. Compr Rev Food Sci Food Saf 7:29–49
Shabala S, Pottosin II (2010) Potassium and potassium-permeable channels in plant salt tolerance. In: Demidchik V, Maathuis F (eds) Ion channels and plant stress responses. Springer, Berlin, pp. 87–110
Skibsted LH (2012) Carotenoids in antioxidant networks. Colorants or radical scavengers. J Agric Food Chem 60:2409–2417
Verslues PE (2016) ABA and cytokinins: challenge and opportunity for plant stress research. Plant Mol Biol 91:629–640
Wang M, Zheng Q, Shen Q, Guo S (2013) The critical role of potassium in plant stress response. Int J Mol Sci 14:7370–7390
Yang Y, Yu X, Song L, An C (2011) ABI4 activates DGAT1 expression in Arabidopsis seedlings during nitrogen deficiency. Plant Physiol 156:873–883
Yoshida K, Igarashi E, Wakatsuki E, Miyamoto K, Hirata K (2004) Mitigation of osmotic and salt stresses by abscisic acid through reduction of stress-derived oxidative damage in Chlamydomonas reinhardtii. Plant Sci 167:1335–1341
Yuan JP, Chen F, Liu X, Li XZ (2002) Carotenoid composition in the green microalga Chlorococcum. Food Chem 76:319–325
Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song CP (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448
Zhekisheva M, Boussiba S, Khozin-Goldberg I, Zarka A, Cohen Z (2002) Accumulation of oleic acid in Haematococcus pluvialis (Chlorophyceae) under nitrogen starvation of high light is correlated with that of astaxanthin esters. J Phycol 38:325–331
Acknowledgments
This study was supported by a grant from the Strategic Research Foundation Grant-aided Project for Private Universities from the Ministry of Education, Culture, Sport, Science, and Technology, Japan (S1411005). This work was supported in part by the Research Institute for Science and Technology of Kogakuin University for a special Grant-in-Aid to earn KAKENHI by the Japan Society for the Promotion of Science.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Saeki, K., Aburai, N., Aratani, S. et al. Salt-stress and plant hormone-like responses for selective reactions of esterified xanthophylls in the aerial microalga Coelastrella sp. KGU-Y002. J Appl Phycol 29, 115–122 (2017). https://doi.org/10.1007/s10811-016-0911-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-016-0911-7