Aluminum relieves fluoride stress through stimulation of organic acid production in Camellia sinensis

Physiology and Molecular Biology of Plants - Tập 26 - Trang 1127-1137 - 2020
Junting Pan1, Dongqin Li1, Jiaojiao Zhu1, Zaifa Shu2, Xiaoli Ye1, Anqi Xing1, Bo Wen1, Yuanchun Ma1, Xujun Zhu1, Wanping Fang1, Yuhua Wang1
1College of Horticulture, Nanjing Agricultural University, Nanjing, China
2Lishui Academy of Agricultural Sciences, Lishui, China

Tóm tắt

Tea plants (Camellia sinensis O. Kuntze) can hyperaccumulate fluoride (F) in leaves. Although, aluminum (Al) can alleviate F toxicity in C. sinensis, the mechanisms driving this process remain unclear. Here, we measured root length, root activity, soluble proteins content, and levels of peroxidase, superoxide dismutase, catalase, malondialdehyde (MDA), and chlorophyll in tea leaves after treatment with different F concentrations. In addition, we focused on the content of organic acids, the gene transcription of malate dehydrogenase (MDH), glycolate oxidase (GO) and citrate synthase (CS) and the relative enzyme activity involved in the tolerance to F in C. sinensis. We also examined the role of Al in this process by analyzing the content of these physiological indicators in tea leaves treated with F and Al. Our results demonstrate that increased MDA content, together with decreased chlorophyll content and soluble proteins are responsible for oxidative damage and metabolism inhibition at high F concentration. Moreover, increased antioxidant enzymes activity regulates ROS damage to protect tea leaves during F stress. Furthermore, exogenous Al alleviated F stress in tea leaves through the regulation of MDA content and antioxidant enzymes activity. In addition, organic acids in exudate stimulated root growth in tea plants exposed to low F concentrations are regulated by MDH, GO, and CS. In addition, Al can stimulate the exudation of organic acids, and may participate in regulating rhizosphere pH of the roots through the interaction with F, eventually leading to the response to F stress in C. sinensis.

Tài liệu tham khảo

Arnon DI (1949) Copper enzymes in isolated chloroplasts. polyphenoloxidase in Beta Vulgaris. Plant Physiol 24:1–15 Arora A, Sairam RK, Srivastava GC (2002) Oxidative stress and antioxidative system in plants. Curr Sci 82:1227–1238 Baunthiyal M, Ranghar S (2014) Physiological and biochemical responses of plants under fluoride stress: an overview. Fluoride 47:287–293 Blagoveshchensky AV, Kologrivova AJ (1945) Growth of roots as stimulated by certain organic acids. Doklady Akademii Nauk Soiuza Sovetskikh Sotsialisticheskikh Respublik 48:440 Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254 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 Cao J, Zhao Y, Liu JW, Xirao RD, Danzeng SB, Daji DW, Yan Y (2003) Brick tea fluoride as a main source of adult fluorosis. Food Chem Toxicol 41:535–542 della Fuente JM, Ramirez Rodriguez V, Cabrera Ponce JL, Herrera Estrella L (1997) Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science 276:1566–1568 Deng W, Luo KM, Li ZG, Yang YW, Hu N, Wu Y (2009) Overexpression of Citrus junos mitochondrial citrate synthase gene in Nicotiana benthamiana confers aluminum tolerance. Planta 230:355–365 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 Ding HY, Wen DN, Fu ZW, Qian HF (2014) The secretion of organic acids is also regulated by factors other than aluminum. Environ Monit Assess 186:1123–1131 Hajiboland R, Rad SB, Barcelo J, Poschenrieder C (2013) Mechanisms of aluminum-induced growth stimulation in tea (Camellia sinensis). J Plant Nutr Soil Sci 176:616–625 Johnson JF, Allan DL, Vance CP (1994) Phosphorus stress-induced proteoid roots show altered metabolism in Lupinus-Albus. Plant Physiol 104:657–665 Khan AR, Cheng Z, Ghazanfar B, Khan MA, Zhu YX (2014) Acetyl salicylic acid and 24-epibrassinolide enhance root activity and improve root morphological features in tomato plants under heat stress. Acta Agric Scand 64:304–311 Kinraide TB, Parker DR, Zobel RW (2005) Organic acid secretion as a mechanism of aluminium resistance: a model incorporating the root cortex epidermis, and the external unstirred layer. J Exp Bot 56:1853–1865 Klug B, Horst WJ (2010) Oxalate exudation into the root-tip water free space confers protection from aluminum toxicity and allows aluminum accumulation in the symplast in buckwheat (Fagopyrum esculentum). New Phytol 187:380–391 Kochian LV, Pineros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195 Li XX, Franceschi VR (1990) Distribution of peroxisomes and glycolate metabolism in relation to calcium oxalate formation in Lemna minor L. Eur J Cell Biol 51:9–16 Li CL, Xu HM, Xu J, Chun XY, Ni DJ (2011) Effects of aluminium on ultrastructure and antioxidant activity in leaves of tea plant. Acta Physiol Plant 33:973–978 Li QF, Zhao J, Zhang J, Dai ZH, Zhang LG (2016) Ectopic expression of the chinese cabbage malate dehydrogenase gene promotes growth and aluminum resistance in Arabidopsis. Front Plant Sci 7:1180 Li D, Shu Z, Ye X, Zhu J, Pan J, Wang W, Chang P, Cui C, Shen J, Fang W, Zhu X, Wang Y (2017a) Cell wall pectin methyl-esterification and organic acids of root tips involve in aluminum tolerance in Camellia sinensis. Plant Physiol Biochem 119:265–274 Li Y, Huang J, Song XW, Zhang ZW, Jiang Y, Zhu YL, Zhao H, Ni DJ (2017b) An RNA-Seq transcriptome analysis revealing novel insights into aluminum tolerance and accumulation in tea plant. Planta 246:91–103 Liang J, Shu T, Lin H (1996) The aluminium complexes in the xylem sap of tea plant. J Chin Agric Soc 34:695–702 (in Chinese) Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408 Lu Y, Guo WF, Yang XQ (2004) Fluoride content in tea and its relationship with tea quality. J Agric Food Chem 52:4472–4476 Mishra S, Srivastava S, Tripathi RD, Kumar R, Seth CS, Gupta DK (2006) Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere 65:1027–1039 Morita A, Yanagisawa O, Maeda S, Takatsu S, Ikka T (2011) Tea plant (Camellia sinensis L.) roots secrete oxalic acid and caffeine into medium containing aluminum. Soil Sci Plant Nutr 57:796–802 Mugai EN, Agong SG, Matsumoto H (2000) Aluminium tolerance mechanisms in Phaseolus vulgaris L.: citrate synthase activity and TTC reduction are well correlated with citrate secretion. Soil Sci Plant Nutr 46:939–950 Mukhopadyay M, Bantawa P, Das A, Sarkar B, Bera B, Ghosh P, Mondal TK (2012) Changes of growth, photosynthesis and alteration of leaf antioxidative defence system of tea [Camellia sinensis (L.) O. Kuntze] seedlings under aluminum stress. Biometals 25:1141–1154 Nagata T, Hayatsu M, Kosuge N (1993) Aluminum kinetics in the tea plant using 27Al and 19F NMR. Phytochemistry 32:771–775 Nardi S, Sessi E, Pizzeghello D, Sturaro A, Rella R, Parvoli G (2002) Biological activity of soil organic matter mobilized by root exudates. Chemosphere 46:1075–1081 Oh MW, Roy SK, Kamal AM, Cho K, Cho SW, Park CS, Choi JS, Komatsu S, Woo SH (2014) Proteome analysis of roots of wheat seedlings under aluminum stress. Mol Biol Rep 41:671–681 Pan JT, Wang WD, Li DQ, Shu ZF, Ye XL, Chang PP, Wang YH (2016) Gene expression profile indicates involvement of NO in Camellia sinensis pollen tube growth at low temperature. BMC Genom 17:809 Ruan JY, Wong MH (2001) Accumulation of fluoride and aluminium related to different varieties of tea plant. Environ Geochem Health 23:53–63 Ruan JY, Ma LF, Shi YZ, Han WY (2003) Uptake of fluoride by tea plant (Camellia sinensis L) and the impact of aluminium. J Sci Food Agric 83:1342–1348 Ruf M, Brunner I (2003) Vitality of tree fine roots: reevaluation of the tetrazolium test. Tree Physiol 23:257–263 Schulze J, Tesfaye M, Litjens RHMG, Bucciarelli B, TreppG Miller S, Samac D, Allan D, Vance CP (2002) Malate plays a central role in plant nutrition. Plant Soil 247:133–139 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 Singh G, Kumari B, Sinam G, Kriti Kumar N, Mallick S (2018) Fluoride distribution and contamination in water, soil and plants continuum and its remedial technologies, an Indian perspective: a review. Environ Pollut 239:95–108 Smith AJ (2001) The bio-availability of fluoride from black tea. J Dent 29:15–21 Unger EA, Hand JM, Cashmore AR, Vasconcelos AC (1989) Isolation of a cDNA encoding mitochondrial citrate synthase from Arabidopsis thaliana. Plant Mol Biol 13:411–418 Wan Q, Xu RK, Li XH (2012) Proton release by tea plant (Camellia sinensis L.) roots as affected by nutrient solution concentration and pH. Plant Soil Environ 58:429–434 Wang P, Bi SP, Ma LP, Han WY (2006) Aluminum tolerance of two wheat cultivars (Brevor and Atlas 66) in relation to their rhizosphere pH and organic acids exuded from roots. J Agric Food Chem 54:10033–10039 Wang SL, Wang P, Wang CY (2010) Changes in rhizosphere pH and exudation of organic acids of masson pine (Pinus massoniana) seedlings under aluminum stress. J Ecol Rural Environ 26:87–91 Wang LX, Tang JH, Xiao B, Yang YJ, Yu YB (2013) Enhanced release of fluoride from rhizosphere soil of tea plants by organic acids and reduced secretion of organic acids by fluoride supply. Acta Agric Scand Sect B Soil Plant Sci 63:426–432 Weber H, Chetelat A, Reymond P, Farmer EE (2004) Selective and powerful stress gene expression in Arabidopsis in response to malondialdehyde. Plant J 37:877–888 Weinstein LH, Halscher-Herman R (1982) Physiological responses of plants to fluorine. In: Effects of gaseous air pollutants in agriculture and horticulture, pp 139–167 Xu HW, Ji XM, He ZH, Shi WP, Zhu GH, Niu JK, Li BS, Peng XX (2006) Oxalate accumulation and regulation is independent of glycolate oxidase in rice leaves. J Exp Bot 9:9 Xu QS, Wang Y, Ding ZT, Fan K, Ma DX, Zhang YL, Yin Q (2017) Aluminum induced physiological and proteomic responses in tea (Camellia sinensis) roots and leaves. Plant Physiol Biochem 115:141–151 Yamada M, Higashiyama T, Kishino S, Kataoka M, Ogawa J, Shirnizu S, Isobe K (2014) Novel alcohol oxidase with glycolate oxidase activity from Ochrobactrum sp. AIU 033. J Mol Catal B Enzymat 105:41–48 Yang Y, Liu Y, Huang CF, Silva JD, Zhao FJ (2016) Aluminium alleviates fluoride toxicity in tea (Camellia sinensis). Plant Soil 402:179–190 Zhang L, Li Q, Ma LF, Ruan JY (2013a) Characterization of fluoride uptake by roots of tea plants (Camellia sinensis (L.) O. Kuntze). Plant Soil 366:659–669 Zhang XC, Gao HJ, Zhang ZZ, Wan XC (2013b) Influence of aluminum on absorption and distribution of fluoride in tea plants (Camellia sinesis L.). Food Science 34:147–150 (in Chinese) Zhang FG, Meng XH, Yang XM, Ran W, Shen QR (2014) Quantification and role of organic acids in cucumber root exudates in Trichoderma harzianum T-E5 colonization. Plant Physiol Biochem 83:250–257