Skip to main content

Advertisement

SpringerLink
Log in

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

  • Research Article
  • Published:
Physiology and Molecular Biology of Plants Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. polyphenoloxidase in Beta Vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arora A, Sairam RK, Srivastava GC (2002) Oxidative stress and antioxidative system in plants. Curr Sci 82:1227–1238

    CAS  Google Scholar 

  • Baunthiyal M, Ranghar S (2014) Physiological and biochemical responses of plants under fluoride stress: an overview. Fluoride 47:287–293

    CAS  Google Scholar 

  • Blagoveshchensky AV, Kologrivova AJ (1945) Growth of roots as stimulated by certain organic acids. Doklady Akademii Nauk Soiuza Sovetskikh Sotsialisticheskikh Respublik 48:440

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Johnson JF, Allan DL, Vance CP (1994) Phosphorus stress-induced proteoid roots show altered metabolism in Lupinus-Albus. Plant Physiol 104:657–665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kochian LV, Pineros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195

    Article  CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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)

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lu Y, Guo WF, Yang XQ (2004) Fluoride content in tea and its relationship with tea quality. J Agric Food Chem 52:4472–4476

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Nagata T, Hayatsu M, Kosuge N (1993) Aluminum kinetics in the tea plant using 27Al and 19F NMR. Phytochemistry 32:771–775

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ruf M, Brunner I (2003) Vitality of tree fine roots: reevaluation of the tetrazolium test. Tree Physiol 23:257–263

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Smith AJ (2001) The bio-availability of fluoride from black tea. J Dent 29:15–21

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Yang Y, Liu Y, Huang CF, Silva JD, Zhao FJ (2016) Aluminium alleviates fluoride toxicity in tea (Camellia sinensis). Plant Soil 402:179–190

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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)

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (no. 31972458, 31770733), the Earmarked Fund for China Agriculture Research System (no. CARS-19), the Earmarked Fund for Jiangsu Agriculture Research System (no. JATS[2019]423).

Author information

Author notes

  1. Junting Pan and Dongqin Li contributed equally.

Authors and Affiliations

  1. College of Horticulture, Nanjing Agricultural University, Nanjing, 210095, China

    Junting Pan, Dongqin Li, Jiaojiao Zhu, Xiaoli Ye, Anqi Xing, Bo Wen, Yuanchun Ma, Xujun Zhu, Wanping Fang & Yuhua Wang

  2. Lishui Academy of Agricultural Sciences, Lishui, 323000, Zhejiang, China

    Zaifa Shu

Authors
  1. Junting Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dongqin Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiaojiao Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zaifa Shu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiaoli Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Anqi Xing
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bo Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yuanchun Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Xujun Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Wanping Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Yuhua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YW, JP and DL conceived the study and wrote the manuscript. DL, ZS and JZ are responsible for the determination of F and Al content and measurement of soluble proteins, POD, SOD, CAT, MDA and chlorophyll content. ZS, DL and JP are responsible for the analyses of organic acids contents and organic acids enzyme activities. JP, XY, JZ and AX were responsible for hydroponic culture and root elongation measurement. XY, JZ and AX were responsible for qRT-PCR experiment and analysis. YW, WF, XZ, BW and YM critically reviewed the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Yuhua Wang.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Primers used for qRT-PCR of MDH, GO, and CS genes in tea plant (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pan, J., Li, D., Zhu, J. et al. Aluminum relieves fluoride stress through stimulation of organic acid production in Camellia sinensis. Physiol Mol Biol Plants 26, 1127–1137 (2020). https://doi.org/10.1007/s12298-020-00813-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12298-020-00813-2

Keywords

Search

Navigation