Physiological and Molecular Mechanisms of Transmembrane Fluoride Uptake by Tea Roots

XU Jiajia; GUANG Min; SHI Shulin; GAO Hongjian

doi:10.13305/j.cnki.jts.2019.04.001

PDF(313 KB)

Journal of Tea Science ›› 2019, Vol. 39 ›› Issue (4) : 365-371. DOI: 10.13305/j.cnki.jts.2019.04.001

Physiological and Molecular Mechanisms of Transmembrane Fluoride Uptake by Tea Roots

XU Jiajia^1,2, GUANG Min², SHI Shulin², GAO Hongjian^1,2,*

Author information +

History +

Abstract

Tea plant is a fluoride hyper-accumulator and most of fluoride is accumulated in the leaves. Drinking tea is an important way to absorb fluoride for human, which affects human health. Fluoride is usually absorbed from the soil by tea roots. However, the physiological and molecular mechanisms of transmembrane fluoride uptake by the tea roots were still poorly documented. Therefore, this paper reviewed the active and passive pathways of fluoride uptake by the roots of tea. The active transmembrane uptake fluoride process and molecular mechanism by H⁺-ATPase and Ca²⁺-ATPase, the role and microscopic process of ion channel and Al-F complexation by passive fluoride uptake were analyzed. The main influencing factors and control measures of fluoride accumulation in tea roots were also investigated. In order to reveal the molecular mechanism of transmembrane fluoride uptake, regulate the selective fluoride uptake in tea roots, and ensure the tea quality and safety for consumption, cloning, expression, and functional verification of transport proteins and genes related to fluoride transmembrane uptake in tea plant should receive more attention in future studies.

Key words

fluoride / influencing factor / physiological and molecular mechanism / tea roots / transmembrane uptake

Cite this article

EndNote

Ris (Procite)

Bibtex

Download Citations

XU Jiajia, GUANG Min, SHI Shulin, GAO Hongjian. Physiological and Molecular Mechanisms of Transmembrane Fluoride Uptake by Tea Roots[J]. Journal of Tea Science. 2019, 39(4): 365-371 https://doi.org/10.13305/j.cnki.jts.2019.04.001

References

[1] Dey S, Giri B.Fluoride fact on human health and health problems: A review[J]. Medical & Clinical Reviews, 2016, 2(1): 2. DOI: 10.21767/2471-299X.1000011.
[2] 张楠, 张凌云. 茶叶中氟的安全性与检测方法研究进展[J]. 茶叶, 2009, 35(1): 3-6.
[3] Weinstein L H, Davison A.Fluorides in the environment: effects on plants and animals[M]. Oxfordshire: CABI, 2004.
[4] Zhang L, Li Q, Ma L, et al.Characterization of fluoride uptake by roots of tea plants (Camellia sinensis, (L.) O. Kuntze)[J]. Plant & Soil, 2013, 366(1/2): 659-669.
[5] Lu Y, Guo W F, Yang X Q.Fluoride content in tea and its relationship with tea quality[J]. Journal of Agricultural and Food Chemistry, 2004, 52(14): 4472-4476.
[6] Shu W S, Zhang Z Q, Lan C Y, et al.Fluoride and aluminium concentrations of tea plants and tea products from Sichuan Province, PR China[J]. Chemosphere, 2003, 52(9): 1475-1482.
[7] 董青华, 孙威江, 杨贤强. 茶树吸收氟的根际效应及富集机理研究进展[J]. 亚热带农业研究, 2009, 5(3): 162-166.
[8] 蔡荟梅, 彭传燚, 李成林, 等. 三个品种茶树氟富集特性及其在亚细胞中的分布[J]. 中国农业科学, 2013, 46(8): 1668-1675.
[9] 彭传燚, 陈静, 蔡荟梅, 等. 茶树对氟的吸收动力学特性研究[J]. 热带作物学报, 2013, 34(3): 495-500.
[10] 王玉梅, 柴如山, 郜红建. 茶树根系跨膜主动吸收氟的表观特征[J]. 农业环境科学学报, 2016, 35(8): 1473-1479.
[11] Li Q S, Lin X M, Qiao R Y, et al.Effect of fluoride treatment on gene expression in tea plant (Camellia sinensis)[J]. Scientific Reports, 2017, 7(1): 9847. DOI: https://www.nature.com/articles/s41598-017-08587-6.
[12] Nagata T, Hayatsu M, Kosuge N.Identification of aluminium forms in tea leaves by ²⁷Al NMR[J]. Phytochemistry, 1992, 31(4): 1215-1218.
[13] Nagata T, Hayatsu M, Kosuge N.Aluminium kinetics in the tea plant using ²⁷Al and ¹⁹F NMR[J]. Phytochemistry, 1993, 32(4): 771-775.
[14] Cao J, Luo S F, Liu J W, et al.Safety evaluation on fluoride content in black tea[J]. Food Chemistry, 2004, 88(2): 233-236.
[15] Yi X Y, Qiao S, Ma L F, et al.Soil fluoride fractions and their bioavailability to tea plants (Camellia sinensis L.)[J]. Environmental Geochemistry & Health, 2017, 39(5): 1005-1016.
[16] 谢忠雷, 陈卓, 孙文田, 等. 不同茶园茶叶氟含量及土壤氟的形态分布[J]. 吉林大学学报(地球科学版), 2008, 38(2): 293-298.
[17] 谢正苗, 吴卫红. 环境中氟化物的迁移和转化及其生态效应[J]. 环境工程学报, 1999(2): 40-53.
[18] Ruan J Y, Wong M H.Accumulation of fluoride and aluminium related to different varieties of tea plant[J]. Environmental Geochemistry and Health, 2001, 23(1): 53-63.
[19] Ruan J T, Ma L, Shi Y, et al.Uptake of fluoride by tea plant (Camellia sinensis L.) and the impact of aluminium[J]. Journal of the Science of Food & Agriculture, 2003, 83(13): 1342-1348.
[20] Horie H, Nagata T, Mukai T, et al.Determination of the chemical form of fluorine in tea infusions by ¹⁹F-NMR[J]. Bioscience Biotechnology and Biochemistry, 1992, 56(9): 1474-1475.
[21] 张显晨, 郜红建, 张正竹, 等. 铝对氟在茶树体内吸收与分配的影响[J]. 食品科学, 2013, 34(5): 147-150.
[22] Palmgren M, Harper J.Pumping with plant P-type ATPases[J]. Journal of Experimental Botany, 1999, 50: 883-893.
[23] Sperandio M V L, Santos L A, Bucher C A, et al. Isoforms of plasma membrane H+-ATPase in rice root and shoot are differentially induced by starvation and resupply of NO₃-, or NH₄+[J]. Plant Science, 2011, 180(2): 251-258.
[24] Teakle N L, Tyerman S D.Mechanisms of Cl- transport contributing to salt tolerance[J]. Plant Cell & Environment, 2010, 33(4): 566-589.
[25] White P J.Ion uptake mechanisms of individual cells and roots: short-distance transport[J]. Marschners Mineral Nutrition of Higher Plants, 2012, 1(5): 7-47.
[26] Shen H, Chen J, Wang Z, et al.Root plasma membrane H+-ATPase is involved in the adaptation of soybean to phosphorus starvation[J]. Journal of Experimental Botany, 2006, 57(6): 1353-1362.
[27] Zhang X C, Gao H J, Yang T Y, et al.Al³+-promoted fluoride accumulation in tea plants (Camellia sinensis) was inhibited by an anion channel inhibitor DIDS[J]. Journal of the Science of Food & Agriculture, 2016, 96(12): 4224-4230.
[28] Pedchenko V K, Nasirova G F, Palladina T A.Lysophosphatidylcholine specifically stimulates plasma membrane H+-ATPase from corn roots[J]. FEBS Letters, 1990, 275(1/2): 205-208.
[29] Pottosin I, Velarde-Buendía A M, Bose J, et al. Polyamines cause plasma membrane depolarization, activate Ca²+-, and modulate H+-ATPase pump activity in pea roots[J]. Journal of Experimental Botany, 2014, 65(9): 2463-2472.
[30] Roberts S K.Plasma membrane anion channels in higher plants and their putative functions in roots[J]. New Phytologist, 2006, 169(4): 647-666.
[31] Zhang X C, Gao H J, Wu H H, et al.Ca²+ and CaM are involved in Al³+ pretreatment-promoted fluoride accumulation in tea plants (Camellia sinesis L.)[J]. Plant Physiology and Biochemistry, 2015, 96: 288-295.
[32] 何龙飞, 刘友良, 沈振国, 等. 植物离子通道特征、功能、调节与分子生物学[J]. 植物学报, 1999, 16(5): 517-525.
[33] Zhang X C, Gao H J, Zhang Z Z, et al.Influences of different ion channel inhibitors on the absorption of fluoride in tea plants (Camellia sinesis L.)[J]. Plant Growth Regulation, 2013, 69(1): 99-106.
[34] Chapman B E, Kuchel P W.Fluoride transmembrane exchange in human erythrocytes measured with ¹⁹F NMR magnetization transfer[J]. European Biophysics Journal, 1990, 19(1): 41-45.
[35] Chen Z, Beck T L.Free energies of ion binding in the bacterial CLC-ec1 chloride transporter with implications for the transport mechanism and selectivity[J]. Journal of Physical Chemistry B, 2016, 120(12): 3129-3139.
[36] Tyerman S D.Anion channels in plants[J]. Annual Review of Plant Biology, 1992, 43(1): 351-373.
[37] 戴松香, 陈少良. 植物根细胞离子通道研究进展[J]. 北京林业大学学报, 2005, 27(3): 98-103.
[38] White P J, Broadley M R.Chloride in soils and its uptake and movement within the plant: a review[J]. Annals of Botany, 2001, 88(6): 967-988.
[39] Stockbridge R B, Robertson J L, Ludmila K P, et al.A family of fluoride-specific ion channels with dual-topology architecture[J]. eLife, 2013, 2: e01084. DOI: 10.7554/eLife.01084.
[40] Stockbridge R B, Lim H H, Otten R, et al.Fluoride resistance and transport by riboswitch-controlled CLC antiporters[J]. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(38): 15289-15294.
[41] Brammer A E, Stockbridge R B, Miller C.F-/Cl- selectivity in CLC^F-type F-/H+ antiporters[J]. The Journal of General Physiology, 2014, 144(2): 129-136.
[42] Berbasova T, Nallur S, Sells T, et al. Fluoride export (FEX) proteins from fungi, plants and animals are ‘single barreled’ channels containing one functional and one vestigial ion pore [J]. Plos One, 2017, 12(5): e0177096. https://doi.org/10.1371/journal.pone.0177096.
[43] Yang Y, Liu Y, Huang C F, et al.Aluminium alleviates fluoride toxicity in tea (Camellia sinensis)[J]. Plant & Soil, 2016, 402(1/2): 179-190.
[44] Xie Z L, Chen Z, et al.Distribution of aluminum and fluoride in tea plant and soil of tea garden in central and southwest China[J]. Chinese Geographical Science, 2007, 17(4): 376-382.
[45] Takmaz-Nisancioglu S, Davison A W.Effects of aluminium on fluoride uptake by plants[J]. New Phytologist, 1988, 109(2): 149-155.
[46] Xie Z M, Ye Z H, Wong M H.Distribution characteristics of fluoride and aluminum in soil profiles of an abandoned tea plantation and their uptake by six woody species[J]. Environment International, 2001, 26(5): 341-346.
[47] Kobayashi T, Nishizawa N K.Iron uptake, translocation, and regulation in higher plants[J]. Ann. rev. plant Biol, 2012, 63(1): 131-152.
[48] 张磊. 茶树氟吸收动力学特性的研究[D]. 北京: 中国农业科学院, 2008.
[49] 吴卫红, 谢正苗, 徐建明, 等. 不同土壤中氟赋存形态特征及其影响因素[J]. 环境科学, 2002, 23(2): 104-108.
[50] Ruan J, Lifeng M A, Shi Y, et al.The impact of pH and calcium on the uptake of fluoride by tea plants (Camellia sinensis L.)[J]. Annals of Botany, 2004, 93(1): 97-105.
[51] Calvo-Polanco M, Zwiazek J J, Jones M D, et al.Effects of NaCl on responses of ectomycorrhizal black spruce (Picea mariana), white spruce (Picea glauca) and jack pine (Pinus banksiana) to fluoride[J]. Physiologia Plantarum, 2009, 135(1): 51-61.
[52] 马立锋, 阮建云, 石元值, 等. 钙[Ca(NO₃)₂和CaO]对茶树氟吸收的影响[J]. 土壤通报, 2005, 36(1): 85-87.
[53] Zhang X C, Gao H J, Yang T Y, et al. Anion channel inhibitor NPPB-inhibited fluoride accumulation in tea plant (Camellia sinensis) is related to the regulation of Ca²⁺, CaM and depolarization of plasma membrane potential [J]. International Journal of Molecular Sciences, 2016, 17(1): 57. https://doi.org/10.3390/ijms17010057.
[54] Santi S, Locci G, Monte R, et al.Induction of nitrate uptake in maize roots: expression of a putative high-affinity nitrate transporter and plasma membrane H+-ATPase isoforms[J]. Journal of Experimental Botany, 2003, 54(389): 1851-1864.
[55] Chang C, Hu Y, Sun S, et al.Proton pump OsA8 is linked to phosphorus uptake and translocation in rice[J]. Journal of Experimental Botany, 2009, 60(2): 557-565.
[56] 王玉梅. 茶树根系跨膜吸收氟的微观机制和转录组学特征[D]. 合肥: 安徽农业大学, 2017.
[57] Facanha A R, De Meis L.Inhibition of maize root H+-ATPase by fluoride and fluoroaluminate complexes[J]. Plant Physiology, 1995, 108(1): 241-246.
[58] Pedersen J T, Falhof J, Ekberg K, et al.Metal fluoride inhibition of a P-type H+ Pump: Stabilization of the phosphoenzyme intermediate contributes to post-translational pump activation[J]. Journal of Biological Chemistry, 2015, 290(33): 20396-20406.
[59] Han N, Ji X L, Du Y P, et. al. Identification of a novel alternative splicing variant of VvPMA1 in grape root under salinity[J]. Frontiers in Plant Science, 2017, 8: 1-10.
[60] 刘艳丽, 金孝芳, 曹丹, 等. 茶树铝、氟富集研究进展[J]. 植物科学学报, 2016, 34(6): 972-977.
[61] 张永利, 王烨军, 廖万有, 等. 施氮对茶园土壤氟和茶树新梢氟含量的影响[J]. 中国生态农业学报, 2015, 23(12): 1562-1570.
[62] Gao H J, Zhang Z Z, Wan X C.Influences of charcoal and bamboo charcoal amendment on soil-fluoride fractions and bioaccumulation of fluoride in tea plants[J]. Environmental Geochemistry and Health, 2012, 34(5): 551-562.