Abstract
Tea plant (Camellia sinensis) may hyperaccumulate fluorine (F) in its leaves, which may cause fluorosis in tea consumers. Recent studies have implied that exogenous calcium (Ca) may reduce F in tea leaves, although our mechanistic understanding of this phenomenon remains limited. Here, the effects of exogenous Ca on the physiological, biochemical and ionic homeostasis of tea leaves were investigated in the presence and absence of F. Elevated levels of malondialdehyde (MDA) and impaired cellular ultrastructure indicated that exogenous F induced stress in tea plants subjected to deficient Ca (0.01, 0.05 mM) and extremely excessive Ca (10 mM) treatments. Additionally, more F were accumulated in leaves compared to the control when tea plants were treated with 0.5 mM Ca. The lowest levels of MDA and F were observed at an optimal level of 5 mM Ca. F increased the levels of caffeine, polyphenols, and catechins, but decreased the content of soluble sugars and gallic acid when the level of Ca was within 5 mM. Moreover, based on a multivariate analysis on ionic composition, the Ca-regulated disorder in the homeostasis of B, Al, Cu, and Zn was strongly correlated with the accumulation of F. Our results demonstrate that within a range of concentrations, exogenous Ca was able to reduce F content and enhance F tolerance in tea leaves. These effects of exogenous Ca on F tolerance may be related to ionic homeostasis.
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References
Ashihara H, Deng W, Mullen W, Crozier A (2010) Distribution and biosynthesisof flavan-3-ols in Camellia sinensis seedlings and expression of genes encoding biosynthetic enzymes. Phytochemistry 71:559–566
Avs P, Hettiarachchy NS (2011) Green tea and grape seed extracts—potential applications in food safety and quality. Food Res Int 44(4):827–839. https://doi.org/10.1016/j.foodres.2011.01.022
Briat JF, Curie C, Gaymard F (2007) Iron utilization and metabolism in plants. Curr Opin Plant Biol 10(3):276–282. https://doi.org/10.1016/j.pbi.2007.04.003
Cai HM, Peng CY, Chen J, Hou RY, Gao HJ, Wan XC (2014) X-ray photoelectron spectroscopy surface analysis of fluoride stress in tea (Camellia sinensis (L.) O. Kuntze) leaves. J Fluorine Chem 158:11–15 https://doi.org/10.1016/j.jfluchem.2013.11.012
Cai HM, Dong YY, Li YY, Li DX, Peng CY, Zhang ZZ, Wan XC (2016) Physiological and cellular responses to fluoride stress in tea (Camellia sinensis) leaves. Acta Physiol Plant 38:144. https://doi.org/10.1007/S11738-016-2156-0
Cao J, Zhao Y, Liu J (1997) Brick tea consumption as the cause of dental fluorosis among children from Mongol, Kazak and Yugu populations in China. Food Chem Toxicol 35:827. https://doi.org/10.1016/S0278-6915(97)00049-5
Cho SC, Chao YY, Kao CH (2012) Calcium deficiency increases Cd toxicity and Ca is required for heat-shock induced Cd tolerance in rice seedlings. J Plant Physiol 169:892–898. https://doi.org/10.1016/j.jplph.2012.02.005
Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212(4):475–486
Dhindsa RS, Plumbdhindsa P, Thorpe TA (1981) Leaf senescence—correlated with increased levels of membrane-permeability and lipid-peroxidation, and decreased levels of superoxide-dismutase and catalase. J Exp Bot 32:93–101. https://doi.org/10.1093/Jxb/32.1.93
Ding ZT, Jia SS, Wang Y, Xiao J, Zhang YF (2017) Phosphate stresses affect ionome and metabolome in tea plants. Plant Physiol Biochem 120:30–39. https://doi.org/10.1016/j.plaphy.2017.09.007
Featherstone JD (1999) Prevention and reversal of dental caries: role of low level fluoride. Community Dent Epidemiol 27(1):31–40
Figueroa CR, Opazo MC, Vera P, Arriagada O, Diaz M, Moya-Leon MA (2012) Effect of postharvest treatment of calcium and auxin on cell wall composition and expression of cell wall-modifying genes in the Chilean strawberry (Fragaria chiloensis) fruit. Food Chem 132:2014–2022 https://doi.org/10.1016/j.foodchem.2011.12.041
Fung KF, Wong MH (2004) Application of different forms of calcium to tea soil to prevent aluminium and fluorine accumulation. J Sci Food Agric 84:1469–1477. https://doi.org/10.1002/jsfa.1842
Gao HJ, Zhao Q, Zhang XC, Wan XC, Mao JD (2014) Localization of fluoride and aluminum in subcellular fractions of tea leaves and roots. J Agric Food Chem 62(10):2313–2319. https://doi.org/10.1021/jf4038437
Ghanati F, Abdolmaleki P, Vaezzadeh M, Rajabbeigi E, Yazdani M (2007) Application of magnetic field and iron in order to change medicinal products of Ocimum basilicum. Environmentalist 27:429–434. https://doi.org/10.1007/s10669-007-9079-7
Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo. Curr Opin Plant Biol 12(3):259–266. https://doi.org/10.1016/j.pbi.2009.04.003
Hepler PK (2005) Calcium: a central regulator of plant growth and development. Plant Cell 17:2142–2155. https://doi.org/10.1105/tpc.105.032508
Hochmal AK, Schulze S, Trompelt K, Hippler M (2015) Calcium-dependent regulation of photosynthesis. BBA-Bioenergetics 1847:993–1003 https://doi.org/10.1016/j.bbabio.2015.02.010
Hu GS, Jia JM, Hur YJ, Chung YS, Lee JH, Yun DJ, Chung DS, Yi GH, Kim TH, Kim DH (2011) Molecular characterization of phenylalanine ammonia lyase gene from cistanche deserticola. Mol Biol Rep 38(6):3741–3750. https://doi.org/10.1007/s11033-010-0489-0
Li C, Zheng Y, Zhou J, Xu J, Ni D (2011) Changes of leaf antioxidant system, photosynthesis and ultrastructure in tea plant under the stress of fluorine. Biol Plant 55:563–566. https://doi.org/10.1007/s10535-011-0126-3
Li Y, Huang J, Song XW, Zhang ZW, Jiang Y, Zhu YL, Zhao H, Ni DJ (2017) An RNA-Seq transcriptome analysis revealing novel insights into aluminum tolerance and accumulation in tea plant. Planta 246:91–103. https://doi.org/10.1007/s00425-017-2688-6
Liang YR, Lu JL, Zhang LY, Wu S, Wu Y (2003) Estimation of black tea quality by analysis of chemical composition and colour difference of tea infusions. Food Chem 80:283–290. https://doi.org/10.1016/S0308-8146(02)00415-6
Liu T, Zhao Q, Gao H, Wan X, Zhang Z (2013) Effects of organic acids and iron plaque outside roots on absorption and accumulation of fluoride in tea plants. J Nanjing Agric Univ 36:72–78
Morgan SH, Maity PJ, Geilfus CM, Lindberg S, Mühling KH (2014) Leaf ion homeostasis and plasma membrane H+-ATPase activity in Vicia faba change after extra calcium and potassium supply under salinity. Plant Physiol Biochem 82(3):244–253. https://doi.org/10.1016/j.plaphy.2014.06.010
Rana NK, Mohanpuria P, Yadav SK (2008) Expression of tea cytosolic glutamine synthetase is tissue specific and induced by cadmium and salt stress. Biol Plant 52(2):361–364. https://doi.org/10.1007/s10535-008-0075-7
Ruan JY, Ma LF, Shi YZ, Han WY (2004) The impact of pH and calcium on the uptake of fluoride by tea plants (Camellia sinensis L.). Ann Bot-London 93:97–105. https://doi.org/10.1093/aob/mch010
Ruiz JM, Bretones G, Baghour M, Ragala L, Belakbir A, Romero L (1998) Relationship between boron and phenolic metabolism in tobacco leaves. Phytochemistry 48(2):269–272
Shi HT, Ye TT, Zhong B, Liu X, Chan ZL (2014) Comparative proteomic and metabolomic analyses reveal mechanisms of improved cold stress tolerance in bermudagrass (Cynodon dactylon (L.) Pers.) by exogenous calcium. J Integr Plant Biol 56:1064–1079. https://doi.org/10.1111/jipb.12167
Shu WS, Zhang ZQ, Lan CY, Wong MH (2003) Fluoride and aluminium concentrations of tea plants and tea products from Sichuan Province, PR. China Chemosphere 52:1475–1482. https://doi.org/10.1016/S0045-6535(03)00485-5
Siddiqui MH, Al-Whaibi MH, Sakran AM, Ali HM, Basalah MO, Faisal M, Alatar AA, Al-Amri AA (2013) Calcium-induced amelioration of boron toxicity in radish. J Plant Growth Regul 32:61–71. https://doi.org/10.1007/s00344-012-9276-6
Singh S, Pandey A, Kumar B, Palni LMS (2010a) Enhancement in growth and quality parameters of tea [Camellia sinensis (L.) O. Kuntze] through inoculation with arbuscular mycorrhizal fungi in an acid soil. Biol Fert Soils 46:427–433. https://doi.org/10.1007/s00374-010-0448-x
Singh DP, Li HL, Øiseth SK, Beloy J, Lundin L, Gidley MJ (2010b) Influence of boron on carrot cell wall structure and its resistance to fracture. J Agric Food Chem 58(16):9181–9189. https://doi.org/10.1021/jf100688t
Tan W, Meng QW, Brestic M, Olsovska K, Yang XH (2011) Photosynthesis is improved by exogenous calcium in heat-stressed tobacco plants. J Plant Physiol 168:2063–2071. https://doi.org/10.1016/j.jplph.2011.06.009
Thanaraj SNS, Seshadri R (1990) Influence of polyphenol oxidase activity and polyphenol content of tea shoot on quality of black tea. J Sci Food Agr 51:57–69. https://doi.org/10.1002/jsfa.2740510107
Wu DZ, Shen QF, Cai SG, Chen ZH, Dai F, Zhang GP (2013) Ionomic responses and correlations between elements and metabolites under salt stress in wild and cultivated barley. Plant Cell Physiol 54:1976–1988. https://doi.org/10.1093/pcp/pct134
Xu SS, Lin SZ, Lai ZX (2015) Cadmium impairs iron homeostasis in arabidopsis thaliana by increasing the polysaccharide contents and the iron-binding capacity of root cell walls. Plant Soil 392(1–2):71–85. https://doi.org/10.1007/s11104-015-2443-3
Yang X, Zhang YZ, Huang BB, Zhang J, Fang YH, Li FX, Zhu CL, Ch HK YQ et al (2015) Effect of fluoride on the biosynthesis of catechins in tea [Camellia sinensis (L.) O. Kuntze] leaves. Sci Hortic-Amsterdam 184:78–84. https://doi.org/10.1016/j.scienta.2014.12.031
Yokosho K, Yamaji N, Ma JF (2011) An al-inducible mate gene is involved in external detoxification of al in rice. Plant J 68(6):1061–1069. https://doi.org/10.1111/j.1365-313X
Zakir Hossain AK, Koyama H, Hara T (2006) Growth and cell wall properties of two wheat cultivars differing in their sensitivity to aluminum stress. J Plant Physiol 163(1):39. https://doi.org/10.1016/j.jplph.2005.02.008
Zaveri NT (2006) Green tea and its polyphenolic catechins: medicinal uses in cancer and noncancer applications. Life Sci 78(18):2073–2080. https://doi.org/10.1016/j.lfs.2005.12.006
Zhang XC, Gao HJ, Wu HH, Yang TY, Zhang ZZ, Mao JD, Wan XC (2015) Ca2+ and CaM are involved in Al3+ pretreatment-promoted fluoride accumulation in tea plants (Camellia sinesis L.). Plant Physiol Biochem 96:288–295. https://doi.org/10.1016/j.plaphy.2015.08.007
Zhang Y, Wang Y, Ding Z, Wang H, Song L, Jia S, Ma D (2017) Zinc stress affects ionome and metabolome in tea plants. Plant Physiol Biochem 111:318–328. https://doi.org/10.1016/j.plaphy.2016.12.014
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This work was financially supported by a grant from National Natural Science Foundation of China (No. 31470691).
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Luo, J., Ni, D., He, C. et al. Influence of exogenous calcium on the physiological, biochemical, phytochemical and ionic homeostasis of tea plants (Camellia sinensis (L.) O. Kuntze) subjected to fluorine stress. Plant Growth Regul 87, 455–465 (2019). https://doi.org/10.1007/s10725-019-00478-2
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DOI: https://doi.org/10.1007/s10725-019-00478-2