Abstract
Thallium (Tl) is a highly toxic element with two species, Tl(I) and Tl(III). We discovered the Tl uptake in rice exposed to Tl(III) hydroponic treatment was significantly lower than that to Tl(I) treatment, but the content of oxalic acid secreted from roots in Tl(III) treatment was higher than that in Tl(I). The physiological and molecular mechanisms underlying the difference between the two Tl species were studied using a hydroponic system. The results showed the reduction of oxalic acid content had no effect on the amount of Tl on the root surface, indicating oxalic acid might not immobilize Tl to affect the Tl uptake. Therefore, the secretion of oxalic acid from roots may not be a strategy for detoxifying Tl in rice. Notably, Tl(III) increased the expression of Oryza sativa H+-ATPase genes OsAs and the activity of H+-ATPase, and decreased potassium transport gene expression of OsKAT1.1 and OsHKT2;4, which indicated that the difference in Tl uptake of rice between the two Tl species mainly cause by the potassium transport system rather than oxalic acid.
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References
Arpadjan S, Petrova P, Knutsson J (2011) Speciation analysis of thallium in water samples after separation/ preconcentration with the Empore (TM) chelating disk. Intern J Environ Anal Chem 91:1088–1099. https://doi.org/10.1080/03067310903359476
Clemens S, Ma L (2016) Toxic heavy metal and metalloid accumulation in crop plants and foods. Anna. Rev. Plant Biol. 67, 489–512. https://doi.org/10.1146/annurev-arplant-043015-112301
Gierth M, Mäser P (2007) Potassium transporters in plants–involvement in K+ acquisition, redistribution and homeostasis. FEBS Lett 581:2348–2356. https://doi.org/10.1016/j.febslet.2007.03.035
Guo C, Chen Q, Zhao X, Chen X, Zhao Y, Wang L, Li K, Yu Y, Chen L (2013) Al-enhanced expression and interaction of 14-3-3 protein and plasma membrane H+-ATPase is related to Al-induced citrate secretion in an Al-resistant black soybean. Plant Mol Biol Rep 31:1012–1024. https://doi.org/10.1007/s11105-013-0569-0
Gupta M, Qiu X, Wang L, Xie W, Zhang C, Xiong L, Lian X, Zhang Q (2008) KT/HAK/KUP potassium transporters gene family and their whole-life cycle expression profile in rice (Oryza sativa). Mol Genet Genomics 280:437–452. https://doi.org/10.1007/s00438-008-0377-7
Hassler C, Chafin R, Klinger M, Twiss M (2007) Application of the biotic ligand model to explain potassium interaction with thallium uptake and toxicity to plankton. Environ Toxicol Chem 26:1139–1145. https://doi.org/10.1897/06-315R.1
Kwan KHM, Smith S (1991) Some aspects of the kinetics of cadmium and thallium uptake by fronds ofLemna minorL. New Phytol. 117:91–102. https://doi.org/10.1111/j.1469-8137.1991.tb00948.x
Li XT, Wang W, Jiang CJ, Li CH, Cao MJ (2010) Root biological responses of low potassium tolerance and sensitive soybean varieties to low-potassium stress. Soybean Sci 29:800–803
Ligaba A, Yamaguchi M, Shen H, Sasaki T, Yamamoto Y, Matsumoto H (2004) Phosphorus deficiency enhances plasma membrane H+-ATPase activity and citrate exudation in greater purple lupin (Lupinus pilosus). Funct Plant Biology 31:1075–1083. https://doi.org/10.1071/FP04091
Loss Sperandio MV, Santos LA, Huertas Tavares OC, Fernandes MS, de Freitas Lima M, de Souza SR (2020) Silencing the Oryza sativa plasma membrane H+-ATPase isoform OsA2 affects grain yield and shoot growth and decreases nitrogen concentration. J Plant Physiol 251:153220. https://doi.org/10.1016/j.jplph.20.20.153220
Musavizadeh Z, Najafi-Zarrini H, Kazemitabar SK, Hashemi SH, Faraji S, Barcaccia G, Heidari P (2021) Genome-wide analysis of Potassium Channel genes in rice: expression of the OsAKT and OsKAT genes under salt stress. Genes 12:784. https://doi.org/10.3390/genes12050784
Nagel AH, Cuss CW, Goss GG, Shotyk W, Glover CN (2019) The effect of major ions and dissolved organic matter on complexation and toxicity of dissolved thallium to Daphnia magna. Environ Toxicol Chem 38:2472–2479. https://doi.org/10.1002/etc.4557
Radić S, Cvjetko P, Glavas K, Pevalek-Kozlina RV, Pavlica B, M (2009) Oxidative stress and DNA damage in broad bean (Vicia faba L.) seedlings induced by thallium. Environ Toxicol Chem 28:189–196. https://doi.org/10.1897/08-188.1
Renkema H, Koopmans A, Hale B, Berkelaar E (2015) Thallium and potassium uptake kinetics and competition differ between durum wheat and canola. Environ Sci Pollut Res 22:2166–2174. https://doi.org/10.1007/s11356-014-3490-7
Ritchie RJ, Larkum AWD, Uptake of thallium, a toxic heavy-metal, in the cyanobacterium synechococcus R-2(Anacystis nidulans, Leopoliensis S(1998)PCC7942. Plant Cell Physiol.39,1156–1168. https://doi.org/10.1093/oxfordjournals.pcp.a029316.
Schmittgen T, Livak K (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108. https://doi.org/10.1038/nprot.2008.73
Shanker A, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31:739–753. https://doi.org/10.1016/j.envint.2005.02.003
Twining B, Twiss M, Fisher N (2003) Oxidation of thallium by freshwater plankton communities. Environ Sci Technol 37:2720–2726. https://doi.org/10.1021/es026145i
Twiss M, Twining B, Fisher N (2004) Bioconcentration of inorganic and organic thallium by freshwater phytoplankton. Environ Toxicol Chem 23:968–973. https://doi.org/10.1897/02-643
Wu Y, Zhang W, Xiao T, Fu C, Ji Q, Xie L (2017) Effect of K deficiency on emergence of root exudates and mobilization of soil potassium in different banana genotypes. Southwest China Journal of Agricultural Sciences 30:624–628. https://doi.org/10.16213/j.cnki.scjas.2017.3.025
Yao Y, Wang M, Zhang P, Wang X, Huang X, Liu W, Wang Z, Yang R (2020) Different responses in metallothionein gene expression and antioxidative enzyme activity lead to more ROS accumulation and toxicity in rice exposed to Tl(III) than to Tl(I). Chemosphere 259:127258. j. chemosphere.2020.127258 https://doi.org/10.1016/j.chemosphere.2020.127258
Yao Y, Zhang F, Wang M, Liu F, Liu W, Li X, Qin D, Geng X, Huang X, Zhang P (2018) Thallium-induced oxalate secretion from rice (Oryza sativa L.) root contributes to the reduction of Tl(III) to Tl(I). Environ Exp Bot 155:387–393. https://doi.org/10.1016/j.envexpbot.2018.07.028
Yu XZ, Ling QL, Li YH, Lin YJ (2018) mRNA analysis of genes encoded with phytochelatin synthase (PCS) in rice seedlings exposed to chromium: the role of phytochelatins in Cr detoxification. Bull Environ Contam Toxicol 101:257–261. https://doi.org/10.1007/s00128-018-2362-0
Yu W, Kan Q, Zhang J, Zeng B, Chen Q (2016) Role of the plasma membrane H(+)-ATPase in the regulation of organic acid exudation under aluminum toxicity and phosphorus deficiency. Plant Signal Behav 11:e1106660. https://doi.org/10.1080/15592324.2015.1106660
Zhang J, Wei J, Li D, Kong X, Rengel Z, Chen L, Yang Y, Cui X, Chen Q (2017) The role of the plasma membrane H+-ATPase in plant responses to aluminum toxicity. 8:1757. https://doi.org/10.3389/fpls.2017.01757.Front Plant Sci.
Zhang Q, Rickaby R (2020) Interactions of thallium with marine phytoplankton. Geochim Cosmochim Ac 276:1–13. https://doi.org/10.1016/j.gca.2020.02.024
Acknowledgements
This work was supported by Guangdong Provincial Key Research Program of Universities (2019KZDXM054), Rural Revitalization Strategy Project of Guangdong Province (620096-3), Guangdong Basic and Applied Basic Research Foundation (2020A1515011440), Guangzhou Science and Technology Project (202102010452; 202102010385) and Guangdong Water Conservancy Science and Technology Innovation Project (2020-33). Dr. Hui Liu (The University of Western Australia, Australia) is thanked for providing language help.
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Yao, Y., Yang, R., Liao, W. et al. Is Oxalic Acid Secretion A Detoxification Strategy for Rice Exposed to Tl(I) or Tl(III)?. Bull Environ Contam Toxicol 109, 920–926 (2022). https://doi.org/10.1007/s00128-022-03613-4
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DOI: https://doi.org/10.1007/s00128-022-03613-4