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Physiological and cellular responses to fluoride stress in tea (Camellia sinensis) leaves

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Abstract

Tea (Camellia sinensis (L.) O. Kuntze) hyper-accumulates fluoride (F), mainly in the leaves. To understand how tea copes with the stress caused by F, we tracked photosynthesis, antioxidant defense, and cell ultrastructure under different F concentrations (0–50 mg L−1). High F (≥5 mg L−1) caused decreases in photosynthetic and chlorophyll fluorescence parameters. Activated oxygen metabolism was altered by F, as manifested in increasing lipid peroxidation, electrolyte leakage (EL), and accumulation of H2O2. The activities of ascorbate peroxidase (APX, EC 1.11.1.1) and catalase (CAT, EC 1.11.1.6) increased at 0–5 mg L−1 F, but sharply decreased less than 10–50 mg L−1 F. The activity of manganese superoxide dismutase (Mn-SOD, EC 1.15.1.1) decreased with increasing F concentration. Expression of genes encoding antioxidant enzymes were in accordance with their measured activities. The results suggest that the antioxidant enzymes in the tea plant can eliminate reactive oxygen species (ROS) at <5 mg L−1 F, but not at 20–50 mg L−1 F. High F increased the number of epidermal hairs on tea leaves and decreased the stomatal aperture, reducing water loss. The leaf cellular structure appeared normal under 1–50 mg L−1 F, although starch grains in chloroplast increased with increasing F. Proline and betaine play important roles in osmotic regulation in tea plant tolerating F stress. ROS scavenging and greater number of epidermal hairs are likely parts of the tea plant F-tolerance mechanism.

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References

  • Amin T, Yahya A, Maziah M, Ahmad S, Zakaria W (2012) Leaf water status, proline content, lipid peroxidation and accumulation of hydrogen peroxide in salinized Chinese kale (Brassica alboglabra). J Food Agric Environ 10:371–374

    Google Scholar 

  • Arora A, Sairam R, Srivastava G (2002) Oxidative stress and antioxidative system in plants. Current Sci India 82:1227–1238

    CAS  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ashraf M, Foolad M (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • Bhatia NP, Walsh KB, Baker AJ (2005) Detection and quantification of ligands involved in nickel detoxification in a herbaceous Ni hyperaccumulator Stackhousia tryonii Bailey. J Exp Bot 56:1343–1349

    Article  CAS  PubMed  Google Scholar 

  • Bosabalidis AM, Kofidis G (2002) Comparative effects of drought stress on leaf anatomy of two olive cultivars. Plant Sci 163:375–379

    Article  CAS  Google Scholar 

  • Cai H, Peng C, Chen J, Hou R, Gao H, Wan X (2014) X-ray photoelectron spectroscopy surface analysis of fluoride stress in tea (Camellia sinensis (L.) O. Kuntze) leaves. J Fluorine Chem 158:11–15

    Article  CAS  Google Scholar 

  • Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plantarum 83:463–468

    Article  CAS  Google Scholar 

  • Chakrabarti S, Patra PK (2013) Effect of fluoride on superoxide dismutase activity in four common crop plants. Fluoride 46:59–61

    CAS  Google Scholar 

  • Dan TV, KrishnaRaj S, Saxena PK (2000) Metal tolerance of scented geranium (Pelargonium sp. ‘Frensham’): effects of cadmium and nickel on chlorophyll fluorescence kinetics. Int J Phytoremediat 2:91–104

    Article  CAS  Google Scholar 

  • Dat JF, Inzé D, Van Breusegem F (2001) Catalase-deficient tobacco plants: tools for in planta studies on the role of hydrogen peroxide. Redox Rep 6:37–42

    Article  CAS  PubMed  Google Scholar 

  • Dey U, Mondal NK, Das K, Dattaa JK (2012) Dual effects of fluoride and calcium on the uptake of fluoride, growth physiology, pigmentation, and biochemistry of bengal gram seedlings (Cicer arietinum L.). Fluoride 45:389–393

    CAS  Google Scholar 

  • Dhindsa RS, Plumb-Dhindsa 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

    Article  CAS  Google Scholar 

  • Elloumi N, Abdallah FB, Mezghani I, Rhouma A, Boukhris M, Tunisia S (2005) Effect of fluoride on almond seedlings in culture solution. Fluoride 38:193

    CAS  Google Scholar 

  • Faisal M, Anis M (2009) Changes in photosynthetic activity, pigment composition, electrolyte leakage, lipid peroxidation, and antioxidant enzymes during ex vitro establishment of micropropagated Rauvolfia tetraphylla plantlets. Plant Cell Tiss Org 99:125–132

    Article  CAS  Google Scholar 

  • Fornasiero RB (2001) Phytotoxic effects of fluorides. Plant Sci 161:979–985

    Article  CAS  Google Scholar 

  • Fornasiero RB (2003) Fluorides effects on Hypericum perforatum plants: first field observations. Plant Sci 165:507–513

    Article  CAS  Google Scholar 

  • Gajić G, Mitrović M, Pavlović P, Stevanović B, Djurdjević L, Kostić O (2009) An assessment of the tolerance of Ligustrum ovalifolium Hassk. to traffic-generated Pb using physiological and biochemical markers. Ecotox Environ Safe 72:1090–1101

    Article  Google Scholar 

  • Gao H, Zhao Q, Zhang X, Wan X, Mao J (2014) Localization of fluoride and aluminum in subcellular fractions of tea leaves and roots. J Agr Food Chem 62:2313–2319

    Article  CAS  Google Scholar 

  • Gautam R, Bhardwaj N (2010) Bioaccumulation of fluoride in different plant parts of Hordeum vulgare (barley) var. rd-2683 from irrigation water. Fluoride 43:57–60

    CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Bioch 48:909–930

    Article  CAS  Google Scholar 

  • Guo Y, Zhou H, Zhang L (2006) Photosynthetic characteristics and protective mechanisms against photooxidation during high temperature stress in two citrus species. Sci Hortic 108:260–267

    Article  CAS  Google Scholar 

  • Gupta N, Meena S, Gupta S, Khandelwal S (2002) Gas exchange, membrane permeability, and ion uptake in two species of Indian jujube differing in salt tolerance. Photosynthetica 40:535–539

    Article  CAS  Google Scholar 

  • Gupta S, Banerjee S, Mondal S (2009) Phytotoxicity of fluoride in the germination of paddy (Oryza sativa) and its effect on the physiology and biochemistry of germinated seedlings. Fluoride 42:142

    CAS  Google Scholar 

  • Islam E, Liu D, Li T, Yang X, Jin X, Mahmood Q, Tian S, Li J (2008) Effect of Pb toxicity on leaf growth, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater 154:914–926

    Article  CAS  PubMed  Google Scholar 

  • Jha S, Nayak A, Sharma Y (2009) Fluoride toxicity effects in onion (Allium cepa L.) grown in contaminated soils. Chemosphere 76:353–356

    Article  CAS  PubMed  Google Scholar 

  • Karbassi P, Garrard L, West S (1971) Reversal of low temperature effects on a tropical plant by gibberellic acid. Crop Sci 11:755–757

    Article  CAS  Google Scholar 

  • Konishi S (1992) Promotive effects of aluminium on tea plant growth. Jpn Agrl Res Q 26:26–33

    CAS  Google Scholar 

  • Kumar KA, Rao AVB (2008) Physiological responses to fluoride in two cultivars of mulberry. World J Agric Sci 4:463–466

    Google Scholar 

  • Küpper H, Zhao F, McGrath SP (1999) Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 119:305–312

    Article  PubMed Central  Google Scholar 

  • Lee S-H, Ahsan N, Lee K-W, Kim D-H, Lee D-G, Kwak S-S, Kwon S-Y, Kim T-H, Lee B-H (2007) Simultaneous overexpression of both CuZn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. J Plant Physiol 164:1626–1638

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Yu L, Deng Y, Li W, Li M, Cao J (2007) Leaf epidermal characters of Lonicera japonica and Lonicera confuse and their ecology adaptation. J Forestry Res 18:103–108

    Article  CAS  Google Scholar 

  • Li C, Xu H, Xu J, Chun X, Ni D (2011a) Effects of aluminium on ultrastructure and antioxidant activity in leaves of tea plant. Acta Physiol Plant 33:973–978

    Article  CAS  Google Scholar 

  • Li C, Zheng Y, Zhou J, Xu J, Ni D (2011b) Changes of leaf antioxidant system, photosynthesis and ultrastructure in tea plant under the stress of fluorine. Biol Plantarum 55:563–566

    Article  CAS  Google Scholar 

  • Lin CC, Kao CH (2000) Effect of NaCl stress on H2O2 metabolism in rice leaves. Plant Growth Regul 30:151–155

    Article  CAS  Google Scholar 

  • Liu D, Kottke I (2004) Subcellular localization of copper in the root cells of Allium sativum by electron energy loss spectroscopy (EELS). Bioresour Technol 94:153–158

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Zhang G, Qi M, Li T (2015) Effects of calcium on photosynthesis, antioxidant system, and chloroplast ultrastructure in tomato leaves under low night temperature stress. J Plant Growth Regul 1–11

  • Mackowiak C, Grossl P, Bugbee B (2003) Biogeochemistry of fluoride in a plant–solution system. J Environ Qual 32:2230–2237

    Article  CAS  PubMed  Google Scholar 

  • McNeil SD, Rhodes D, Russell BL, Nuccio ML, Shachar-Hill Y, Hanson AD (2000) Metabolic modeling identifies key constraints on an engineered glycine betaine synthesis pathway in tobacco. Plant Physiol 124:153–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mishra S, Srivastava S, Tripathi R, Kumar R, Seth C, Gupta D (2006) Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere 65:1027–1039

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Pereira GJG, Molina SMG, Lea PJ, Azevedo RA (2002) Activity of antioxidant enzymes in response to cadmium in Crotalaria juncea. Plant Soil 239:123–132

    Article  CAS  Google Scholar 

  • Ruan J, Wong MH (2001) Accumulation of fluoride and aluminium related to different varieties of tea plant. Environ Geochem and Hlth 23:53–63

    Article  CAS  Google Scholar 

  • Ruan J, Ma L, Shi Y, Han W (2004) The impact of pH and calcium on the uptake of fluoride by tea plants (Camellia sinensis L.). Ann Bot 93:97–105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saini P, Khan S, Baunthiyal M, Sharma V (2013) Effects of fluoride on germination, early growth and antioxidant enzyme activities of legume plant species Prosopis juliflora. J Environ Biol 34:205–209

    PubMed  Google Scholar 

  • Shu W, Zhang Z, Lan C, Wong M (2003) Fluoride and aluminium concentrations of tea plants and tea products from Sichuan Province, PR China. Chemosphere 52:1475–1482

    Article  CAS  PubMed  Google Scholar 

  • Singh M, Verma KK (2013) Influence of fluoride-contaminated irrigation water on physiological responses of poplar seedlings (Populus deltoides L. clone-S 7 C 15). Fluoride 46:83–89

    CAS  Google Scholar 

  • Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28:1057–1060

    Article  CAS  Google Scholar 

  • Tingey DT, Hogsett WE (1985) Water stress reduces ozone injury via a stomatal mechanism. Plant Physiol 77:944–947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weinstein LH, Davison A (2004) Fluorides in the environment: effects on plants and animals. CABI

  • Xie Z, Chen Z, Sun W, Guo X, Yin B, Wang J (2007) Distribution of aluminum and fluoride in tea plant and soil of tea garden in Central and Southwest China. Chinese Geogr Sci 17:376–382

    Article  Google Scholar 

  • Yamagishi M (1998) Effects of culture temperature on the enlargement, sugar uptake, starch accumulation, and respiration of in vitro bulblets of Lilium japonicum Thunb. Sci Hortic 73:239–247

    Article  CAS  Google Scholar 

  • Yang S, Miller G (1963) Biochemical studies on the effect of fluoride on higher plants. 1. Metabolism of carbohydrates, organic acids and amino acids. Biochem J 88:505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang D, Liu Y, Sun M, Zhao L, Wang Y, Chen X, Wei C, Gao L, Xia T (2012) Differential gene expression in tea (Camellia sinensis L.) calli with different morphologies and catechin contents. J Plant Physiol 169:163–175

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Hu C, Yao J (2010) Tetraploidization of diploid Dioscorea results in activation of the antioxidant defense system and increased heat tolerance. J Plant Physiol 167:88–94

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Jiang X, Li T, Cao X (2014a) Photosynthesis and ultrastructure of photosynthetic apparatus in tomato leaves under elevated temperature. Photosynthetica 52:430–436

    Article  CAS  Google Scholar 

  • Zhang Z, Ma M, Liu X, Ma R, Liu J (2014b) Structural and ultra-structural disorders in Ziziphus jujuba Miller fruits under fluorine stress. Fluoride 47:208–226

    Google Scholar 

Download references

Acknowledgments

The present work was financially supported by the Earmarked Fund for Modern Agro-industry Technology Research System in Tea Industry (CARS-23, the Ministry of Agriculture of P. R. China), Anhui Major Demonstration Project for Leading Talent Team on Tea Chemistry and Health, Natural Science Foundation of Anhui Province (1408085MKL38), Anhui Scientific and Technological Project (1406C085017), and Changjiang Scholars and Innovative Research Team in University (IRT1101).

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Authors and Affiliations

  1. State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, 130 West Changjiang Road, Hefei, 230036, People’s Republic of China

    Huimei Cai, Yangyang Dong, Yeyun Li, Daxiang Li, Chuanyi Peng, Zhengzhu Zhang & Xiaochun Wan

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  1. Huimei Cai
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  2. Yangyang Dong
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Correspondence to Xiaochun Wan.

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Communicated by A. Krolicka.

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Cai, H., Dong, Y., Li, Y. et al. Physiological and cellular responses to fluoride stress in tea (Camellia sinensis) leaves. Acta Physiol Plant 38, 144 (2016). https://doi.org/10.1007/s11738-016-2156-0

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  • DOI: https://doi.org/10.1007/s11738-016-2156-0

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