Abstract
Cadmium (Cd) is absorbed readily by rice plants and is transferred to humans when contaminated rice is consumed. Adding selenium (Se) to the plant nutrient solutions reduces the accumulation of Cd in the rice (Oryza sativa L.) seedlings. However, as the relevant underlying mechanism remains unclear, the aim of our study was to improve our understanding of the Se-mediated resistance to Cd stress in rice. We conducted hydroponic experiments to study the effects of selenite or selenate on Cd subcellular distribution and xylem transport in rice seedlings under Cd stress, and we investigated the antioxidative defense responses in the rice plants. We found that the supplementation of both Se forms decreased the Cd accumulations in the roots and shoots of the rice plants. The selenite addition significantly decreased the Cd contents in different subcellular fractions of the rice roots, increased the proportion of Cd distributed to soluble cytosol by 23.41%, and decreased the Cd distribution in the organelle by 28.74% in contrast with the treatment with Cd only. As regards the selenate addition, only the Cd distribution ratio of cytosol was increased by 13.07%. After adding selenite, a decrease of 55.86% in the Cd concentration in xylem sap was observed, whereas little change was found after treatment co-applied with selenate. The hydrogen peroxide (H2O2) and malondialdehyde(MDA) contents in the rice roots were elevated under Cd stress, and the addition of selenite and selenate decreased the H2O2 levels by 77.78% and 59.26%, respectively. Co-exposure to Cd and Se elevated the glutathione (GSH) accumulations in the rice shoots and roots, with the degree of increase being the following: co-applied with selenite > co-applied with selenate > Cd alone treatment. Exposure to Cd increased the catalase (CAT) activity in the roots significantly, whereas it decreased in the shoots. After selenite or selenate supplementation, the CAT activity in the rice roots increased compared with applying only Cd. Compared with the control, the addition of Cd or Se had no significant effect on the activities of peroxidase (POD) or ascorbate peroxidase (APX). Our results showed that Se affected the Cd accumulation in rice seedlings by altering the Cd subcellular distribution and decreasing the ROS induced by Cd stress. Such effects were more significant in the selenite than in the selenate applied treatment.
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References
Badiello R, Feroci G, Fini A (1996) Interaction between trace elements: selenium and cadmium ions. J Trace Elem Med Biol 10:156–162. https://doi.org/10.1016/S0946-672X(96)80026-5
Brown KM, Arthur JR (2001) Selenium, selenoproteins and human health: a review. Public Health Nutr 4:593–599
Chen CH, Zhou QX, Cai Z, Wang YY (2010) Effects of soil polycyclic musk and cadmium on pollutant uptake and biochemical responses of wheat (Triticum aestivum). Arch Environ Contam Toxicol 59:564–573. https://doi.org/10.1007/s00244-010-9522-5
Chen CH, Zhou Q, Cai Z (2014) Effect of soil HHCB on cadmium accumulation and phytotoxicity in wheat seedlings. Ecotoxicol 23:1996–2004. https://doi.org/10.1007/s10646-014-1317-4
Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719. https://doi.org/10.1016/j.biochi.2006.07.003
Cui JH, Liu TX, Li FB, Yi JC, Liu CP, Yu HY (2017) Silica nanoparticles alleviate cadmium toxicity in rice cells: mechanisms and size effects. Environ Pollut 228:363–369. https://doi.org/10.1016/j.envpol.2017.05.014
DalCorso G, Farinati S, Maistri S, Furini A (2008) How plants cope with cadmium: staking all on metabolism and gene expression. J Integr Plant Biol 50:1268–1280. https://doi.org/10.1111/j.1744-7909.2008.00737.x
de Souza MP, Pilon-Smits EAH, Lytle CM, Hwang S, Tai J, Honma TSU, Yeh L, Terry N (1998) Rate-limiting steps in selenium assimilation and volatilization by Indian mustard. Plant Physiol 117:1487–1494. https://doi.org/10.1104/pp.117.4.1487
Deuticke B (1989) Oxidative membrane damage—a problem of lipid-peroxidation. Biol Chem H-S 370:618–618
Ding YZ, Feng RW, Wang RG, Guo JK, Zheng XQ (2014) A dual effect of Se on Cd toxicity: evidence from plant growth, root morphology and responses of the antioxidative systems of paddy rice. Plant Soil 375:289–301. https://doi.org/10.1007/s11104-013-1966-8
Djanaguiraman M, Prasad PVV, Seppanen M (2010) Selenium protects sorghum leaves from oxidative damage under high temperature stress by enhancing antioxidant defense system. Plant Physiol Biochem 48:999–1007. https://doi.org/10.1016/j.plaphy.2010.09.009
Dong J, Mao W, Zhang G, Wu F, Cai Y (2007) Root excretion and plant tolerance to cadmium toxicity—a review. Plant Soil Environ 53:193
Du Y, Hu XF, Wu XH, Shu Y, Jiang Y, Yan XJ (2013) Effects of mining activities on Cd pollution to the paddy soils and rice grain in Hunan province, Central South China. Environ Monit Assess 185:9843–9856. https://doi.org/10.1007/s10661-013-3296-y
Feng RW, Wei CY, Tu SX, Tang SR, Wu FC (2011) Simultaneous hyperaccumulation of arsenic and antimony in Cretan brake fern: evidence of plant uptake and subcellular distributions. Microchem J 97:38–43. https://doi.org/10.1016/j.microc.2010.05.010
Feng RW, Wei CY, Tu SX (2013a) The roles of selenium in protecting plants against abiotic stresses. Environ Exp Bot 87:58–68. https://doi.org/10.1016/j.envexpbot.2012.09.002
Feng RW, Wei CY, Tu SX, Ding YZ, Song ZG (2013b) A dual role of Se on Cd toxicity: evidences from the uptake of Cd and some essential elements and the growth responses in paddy rice. Biol Trace Elem Res 151:113–121. https://doi.org/10.1007/s12011-012-9532-4
Filek M, Keskinen R, Hartikainen H, Szarejko I, Janiak A, Miszalski Z, Golda A (2008) The protective role of selenium in rape seedlings subjected to cadmium stress. J Plant Physiol 165:833–844. https://doi.org/10.1016/j.jplph.2007.06.006
Filek M, Zembala M, Hartikainen H, Miszalski Z, Kornas A, Wietecka-Posluszny R, Walas P (2009) Changes in wheat plastid membrane properties induced by cadmium and selenium in presence/absence of 2,4-dichlorophenoxyacetic acid. Plant Cell Tissue Organ Cult 96:19–28. https://doi.org/10.1007/s11240-008-9455-0
Filek M, Gzyl-Malcher B, Zembala M, Bednarska E, Laggner P, Kriechbaum M (2010) Effect of selenium on characteristics of rape chloroplasts modified by cadmium. J Plant Physiol 167:28–33. https://doi.org/10.1016/j.jplph.2009.07.003
Freeman JL, Tamaoki M, Stushnoff C, Quinn CF, Cappa JJ, Devonshire J, Fakra SC, Marcus MA, McGrath SP, Hoewyk DV, Pilon-Smits EAH (2010) Molecular mechanisms of selenium tolerance and hyperaccumulation in Stanleya pinnata. Plant Physiol 153:1630–1652. https://doi.org/10.1104/pp.110.156570
Fry SC (1986) Cross-linking of matrix polymers in the growing cell walls of angiosperms. Annu Rev Plant Physiol 37:165–186. https://doi.org/10.1146/annurev.pp.37.060186.001121
He JL, Qin JJ, Long LY, Ma YL, Li H, Li K, Jiang XN, Liu TX, Polle A, Liang ZS, Luo ZB (2011) Net cadmium flux and accumulation reveal tissue-specific oxidative stress and detoxification in Populus × canescens. Physiol Plant 143:50–63. https://doi.org/10.1111/j.1399-3054.2011.01487.x
Jimenez A, Hernandez JA, Pastori G, del Rio LA, Sevilla F (1998) Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiol 118:1327–1335. https://doi.org/10.1104/pp.118.4.1327
Jinadasa N, Collins D, Holford P, Milham PJ, Conroy JP (2016) Reactions to cadmium stress in a cadmium-tolerant variety of cabbage (Brassica oleracea L.): is cadmium tolerance necessarily desirable in food crops? Environ Sci Pollut Res 23:5296–5306. https://doi.org/10.1007/s11356-015-5779-6
Kumar M, Bijo AJ, Baghel RS, Reddy CR, Jha B (2012) Selenium and Spermine alleviates cadmium induced toxicity in the red seaweed Gracilaria dura by regulating antioxidant system and DNA methylation. Plant Physiol Biochem 51:129–138. https://doi.org/10.1016/j.plaphy.2011.10.016
Li H, Luo N, Li YW, Cai QY, Li HY, Mo CH, Wong MH (2017) Cadmium in rice: transport mechanisms, influencing factors, and minimizing measures. Environ Pollut 224:622–630. https://doi.org/10.1016/j.envpol.2017.01.087
Lin R, Wang X, Luo Y, Du W, Guo H, Yin D (2007) Effects of soil cadmium on growth, oxidative stress and antioxidant system in wheat seedlings (Triticum aestivum L.). Chemosphere 69:89–98. https://doi.org/10.1016/j.chemosphere.2007.04.041
Lin L, Zhou WH, Dai HX, Cao FB, Zhang GP, Wu FB (2012) Selenium reduces cadmium uptake and mitigates cadmium toxicity in rice. J Hazard Mater 235– 236:343–351. https://doi.org/10.1016/j.jhazmat.2012.08.012
Liu Y, Barber DS, Zhang P, Liu B (2013) Complex II of the mitochondrial respiratory chain is the key mediator of divalent manganese-induced hydrogen peroxide production in microglia. Toxicol Sci 132:298–306. https://doi.org/10.1093/toxsci/kfs344
Liu WX, Shang SH, Feng X, Zhang GP, Wu FB (2015) Modulation of exogenous selenium in cd-induced changes in antioxidative metabolism, Cd uptake and photosynthetic performance in the two tobacco genotypes differing in Cd tolerance. Environ Toxicol Chem 34:92–99. https://doi.org/10.1002/etc.2760
Lu SC (1999) Regulation of hepatic glutathione synthesis: current concepts and controversies. FASEB J 13:1169–1183
Lux A, Martinka M, Vaculik M, White PJ (2011) Root responses to cadmium in the rhizosphere: a review. J Exp Bot 62:21–37. https://doi.org/10.1093/jxb/erq281
Ma J, Cai H, He C, Zhang W, Wang L (2015) A hemicellulose-bound form of silicon inhibits cadmium ion uptake in rice (Oryza sativa) cells. New Phytol 206:1063–1074. https://doi.org/10.1111/nph.13276
Malik JA, Goel S, Kaur N, Sharma S, Singh I, Nayyar H (2012) Selenium antagonizes the toxic effects of arsenic on mungbean (Phaseolus aureus Roxb.) plants by restricting its uptake and enhancing the antioxidative and detoxification mechanisms. Environ Exp Bot 77:242–248. https://doi.org/10.1016/j.envexpbot.2011.12.001
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Mozafariyan M, Shekari L, Hawrylak-Nowak B, Kamelmanesh MM (2014) Protective role of selenium on pepper exposed to cadmium stress during reproductive stage. Biol Trace Elem Res 160:97–107. https://doi.org/10.1007/s12011-014-0028-2
Mroczek-Zdyrska M, Wojcik M (2011) The influence of selenium on root growth and oxidative stress induced by lead in Vicia faba L. minor plants. Biol Trace Elem Res 147:320–328. https://doi.org/10.1007/s12011-011-9292-6
Poghosyan GH, Mukhaelyan ZH, Vardevanyan PH (2014) Influence of cadmium ions on growth and antioxidant system activity of wheat (Triticum aestivum L.) seedlings. Int J Sci Res Environ Sci 2:371–378. https://doi.org/10.12983/ijsres-2014-p0371-0378
Qiu Q, Wang YT, Yang ZY, Yuan JG (2011) Effects of phosphorus supplied in soil on subcellular distribution and chemical forms of cadmium in two Chinese flowering cabbage (Brassica parachinensis L.) cultivars differing in cadmium accumulation. Food Chem Toxicol 49:2260–2267. https://doi.org/10.1016/j.fct.2011.06.024
Rizwan M, Ali S, Adrees M, Ibrahim M, Tsang DCW, Zia-Ur-Rehman M, Zahir ZA, Rinklebe J, Tack FMG, Ok YS (2017) A critical review on effects, tolerance mechanisms and management of cadmium in vegetables. Chemosphere 182:90–105. https://doi.org/10.1016/j.chemosphere.2017.05.013
Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas MC, Del Rio LA (2001) Regulation of growth, development and whole organism physiology. Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52:2115–2126. https://doi.org/10.1093/jexbot/52.364.2115
Schiavon M, Berto C, Malagoli M, Trentin A, Sambo P, Dall’Acqua S, Pilon-Smits EA (2016) Selenium biofortification in radish enhances nutritional quality via accumulation of methyl-selenocysteine and promotion of transcripts and metabolites related to glucosinolates, phenolics, and amino acids. Front Plant Sci 7:1371. https://doi.org/10.3389/fpls.2016.01371
Shanker K, Mishra S, Srivastava S, Srivastava R, Dass S, Prakash S, Prakash MM (1995) Effect of selenite and selenate on plant uptake of cadmium by kidney bean (Phaseolus mungo) with reference to Cd-Se interaction. Chem Speciat Bioavailab 7:97–100. https://doi.org/10.1080/09542299.1995.11083251
Sors TG, Ellis DR, Salt DE (2005) Selenium uptake, translocation, assimilation and metabolic fate in plants. Photosynth Res 86:373–389. https://doi.org/10.1007/s11120-005-5222-9
Sun HY, Dai HX, Wang XY, Wang GH (2016) Physiological and proteomic analysis of selenium-mediated tolerance to Cd stress in cucumber (Cucumis sativus L.). Ecotoxicol Environ Saf 133:114–126. https://doi.org/10.1016/j.ecoenv.2016.07.003
Terry N, Zayed AM, de Souza MP, Tarun AS (2000) Selenium in higher plants. Annu Rev Plant Physiol Mol Biol 51:401–432. https://doi.org/10.1146/annurev.arplant.51.1.401
Uraguchi S, Fujiwara T (2012) Cadmium transport and tolerance in rice: perspectives for reducing grain cadmium accumulation. Rice 5:1–8. https://doi.org/10.1186/1939-8433-5-5
Vögeli-Lange R, Wagner GJ (1990) Subcellular localization of cadmium and cadmium-binding peptides in tobacco leaves implication of a transport function for cadmium-binding peptides. Plant Physiol 92:1086–1093. https://doi.org/10.1104/pp.92.4.1086
Wan YN, Yu Y, Wang Q, Qiao YH, Li HF (2016) Cadmium uptake dynamics and translocation in rice seedling: influence of different forms of selenium. Ecotoxicol Environ Saf 133:127–134. https://doi.org/10.1016/j.ecoenv.2016.07.001
Wang X, Tam NF, Fu S, Ametkhan A, Ouyang Y, Ye ZH (2014) Selenium addition alters mercury uptake, bioavailability in the rhizosphere and root anatomy of rice (Oryza sativa). Ann Bot 114:271–278. https://doi.org/10.1093/aob/mcu117
Williams PN, Lei M, Sun GX, Huang Q, Lu Y, Deacon C, Meharg AA, Zhu YG (2009) Occurrence and partitioning of cadmium, arsenic and lead in mine impacted paddy rice: Hunan, China. Environ Sci Technol 43:637–642. https://doi.org/10.1021/es802412r
Wu ZC, Wang FH, Liu S, Du YQ, Li FR, Du RY, Wen D, Zhao J (2017) Comparative responses to silicon and selenium in relation to antioxidant enzyme system and the glutathione-ascorbate cycle in flowering Chinese cabbage (Brassica campestris, L. ssp. chinensis, var. utilis) under cadmium stress. Environ Exp Bot 133:1–11. https://doi.org/10.1016/j.envexpbot.2016.07.012
Yu Y, Yuan SL, Zhuang J, Wan YN, Wang Q, Zhang JS, Li HF (2018) Effect of selenium on the uptake kinetics and accumulation of and oxidative stress induced by cadmium in Brassica chinensis. Ecotoxicol Environ Saf 162:571–580. https://doi.org/10.1016/j.ecoenv.2018.07.041
Zhao J, Gao Y, Li YF, HuY PX, Dong Y, Li B, Chen CY, Chai ZF (2013) Selenium inhibits the phytotoxicity of mercury in garlic (Allium sativum). Environ Res 125:75–81. https://doi.org/10.1016/j.envres.2013.01.01
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Wan, Y., Wang, K., Liu, Z. et al. Effect of selenium on the subcellular distribution of cadmium and oxidative stress induced by cadmium in rice (Oryza sativa L.). Environ Sci Pollut Res 26, 16220–16228 (2019). https://doi.org/10.1007/s11356-019-04975-9
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DOI: https://doi.org/10.1007/s11356-019-04975-9