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Silicon has opposite effects on the accumulation of inorganic and methylated arsenic species in rice

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Abstract

Background and aims

Rice (Oryza sativa) is a main source of human exposure to inorganic arsenic and mitigation measures are needed to decrease As accumulation in this staple crop. It has been shown that silicon decreases the accumulation of arsenite but, unexpectedly, increases the accumulation of dimethylarsinic acid (DMA) in rice grain. The aim of this study was to investigate why Si increases DMA accumulation.

Methods

Pot and incubation experiments were conducted to investigate how the addition of sparingly soluble silicate gel affected As speciation in the soil solution and the accumulation of different As species in rice tissues.

Results

Silicon addition significantly decreased the concentration of inorganic As (mainly arsenite) but increased the concentration of DMA in both the vegetative and reproductive tissues of rice. Silicon increased the concentration of DMA in the soil solution, whereas autoclaving soil decreased DMA concentration. Less DMA was adsorbed by the soil than arsenate and Si addition significantly inhibited DMA adsorption.

Conclusions

Silicon increased DMA accumulation and decreased arsenite accumulation in rice through different mechanisms. Silicic acid released from the silicate gel increased the availability of DMA for rice uptake by inhibiting DMA adsorption on the soil solid phase or by displacing adsorbed DMA. Although silicic acid also increased the concentration of inorganic As in the soil solution, this effect was much smaller than the inhibitory effect of Si on arsenite uptake by rice roots.

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References

  • Arao T, Kawasaki A, Baba K, Matsumoto S (2011) Effects of arsenic compound amendment on arsenic speciation in rice grain. Environ Sci Technol 45:1291–1297

    Article  CAS  PubMed  Google Scholar 

  • Bogdan K, Schenk MK (2008) Arsenic in Rice (Oryza sativa L.) related to dynamics of arsenic and silicic acid in daddy soils. Environ Sci Technol 42:7885–7890

    Article  CAS  PubMed  Google Scholar 

  • Carey AM, Scheckel KG, Lombi E, Newville M, Choi Y, Norton GJ, Charnock JM, Feldmann J, Price AH, Meharg AA (2010) Grain unloading of arsenic species in rice. Plant Physiol 152:309–319

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • European Food Safety Authority (2009) Scientific opinion on arsenic in food. EFSA J 7:1351

    Google Scholar 

  • Fleck AT, Mattusch J, Schenk MK (2013) Silicon decreases the arsenic level in rice grain by limiting arsenite transport. J Plant Nutr Soil Sci 176:785–794

    CAS  Google Scholar 

  • Hansen HR, Raab A, Price AH, Duan GL, Zhu YG, Norton GJ, Feldmann J, Meharg AA (2011) Identification of tetramethylarsonium in rice grains with elevated arsenic content. J Environ Monitor 13:32–34

    Article  CAS  Google Scholar 

  • Jia Y, Huang H, Sun GX, Zhao FJ, Zhu YG (2012) Pathways and relative contributions to arsenic volatilization from rice plants and paddy soil. Environ Sci Technol 46:8090–8096

    Article  CAS  PubMed  Google Scholar 

  • Khan MA, Stroud JL, Zhu YG, McGrath SP, Zhao FJ (2010) Arsenic bioavailability to rice is elevated in Bangladeshi paddy soils. Environ Sci Technol 44:8515–8521

    Article  CAS  PubMed  Google Scholar 

  • Li RY, Ago Y, Liu WJ, Mitani N, Feldmann J, McGrath SP, Ma JF, Zhao FJ (2009a) The rice aquaporin Lsi1 mediates uptake of methylated arsenic species. Plant Physiol 150:2071–2080

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li RY, Stroud JL, Ma JF, McGrath SP, Zhao FJ (2009b) Mitigation of arsenic accumulation in rice with water management and silicon fertilization. Environ Sci Technol 43:3778–3783

    Article  CAS  PubMed  Google Scholar 

  • Lomax C, Liu WJ, Wu LY, Xue K, Xiong J, Zhou JZ, McGrath SP, Meharg AA, Miller AJ, Zhao FJ (2012) Methylated arsenic species in plants originate from soil microorganisms. New Phytol 193:665–672

    Article  CAS  PubMed  Google Scholar 

  • Lombi E, Scheckel KG, Pallon J, Carey AM, Zhu YG, Meharg AA (2009) Speciation and distribution of arsenic and localization of nutrients in rice grains. New Phytol 184:193–201

    Article  CAS  PubMed  Google Scholar 

  • Luxton TP, Eick MJ, Rimstidt DJ (2008) The role of silicate in the adsorption/desorption of arsenite on goethite. Chem Geol 252:125–135

    Article  CAS  Google Scholar 

  • Luxton TP, Tadanier CJ, Eick MJ (2006) Mobilization of arsenite by competitive interaction with silicic acid. Soil Sci Soc Amer J 70:204–214

    Article  CAS  Google Scholar 

  • Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M (2006) A silicon transporter in rice. Nature 440:688–691

    Article  CAS  PubMed  Google Scholar 

  • Ma JF, Yamaji N, Mitani N, Tamai K, Konishi S, Fujiwara T, Katsuhara M, Yano M (2007) An efflux transporter of silicon in rice. Nature 448:209–212

    Article  CAS  PubMed  Google Scholar 

  • Ma JF, Yamaji N, Mitani N, Xu XY, Su YH, McGrath SP, Zhao FJ (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci U S A 105:9931–9935

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Meharg AA, Williams PN, Adomako E, Lawgali YY, Deacon C, Villada A, Cambell RCJ, Sun G, Zhu YG, Feldmann J, Raab A, Zhao FJ, Islam R, Hossain S, Yanai J (2009) Geographical variation in total and inorganic arsenic content of polished (white) rice. Environ Sci Technol 43:1612–1617

    Article  CAS  PubMed  Google Scholar 

  • Meharg AA, Zhao FJ (2012) Arsenic & Rice. Springer, Dordrecht, p 171

    Book  Google Scholar 

  • Panaullah GM, Alam T, Hossain MB, Loeppert RH, Lauren JG, Meisner CA, Ahmed ZU, Duxbury JM (2009) Arsenic toxicity to rice (Oryza sativa L.) in Bangladesh. Plant Soil 317:31–39

    Article  CAS  Google Scholar 

  • Raab A, Williams PN, Meharg A, Feldmann J (2007) Uptake and translocation of inorganic and methylated arsenic species by plants. Environ Chem 4:197–203

    Article  CAS  Google Scholar 

  • Seyfferth AL, Fendorf S (2012) Silicate mineral impacts on the uptake and storage of arsenic and plant nutrients in rice (Oryza sativa L.). Environ Sci Technol 46:13176–13183

    Article  CAS  PubMed  Google Scholar 

  • Stroud JL, Khan MA, Norton GJ, Islam MR, Dasgupta T, Zhu YG, Price AH, Meharg AA, McGrath SP, Zhao FJ (2011) Assessing the labile arsenic pool in contaminated paddy soils by isotopic dilution techniques and simple extractions. Environ Sci Technol 45:4262–4269

    Article  CAS  PubMed  Google Scholar 

  • Su YH, McGrath SP, Zhao FJ (2010) Rice is more efficient in arsenite uptake and translocation than wheat and barley. Plant Soil 328:27–34

    Article  CAS  Google Scholar 

  • Swedlund PJ, Webster JG (1999) Adsorption and polymerisation of silicic acid on ferrihydrite, and its effect on arsenic adsorption. Water Res 33:3413–3422

    Article  CAS  Google Scholar 

  • Williams PN, Price AH, Raab A, Hossain SA, Feldmann J, Meharg AA (2005) Variation in arsenic speciation and concentration in paddy rice related to dietary exposure. Environ Sci Technol 39:5531–5540

    Article  CAS  PubMed  Google Scholar 

  • Williams PN, Raab A, Feldmann J, Meharg AA (2007a) Market basket survey shows elevated levels of As in South Central US processed rice compared to California: Consequences for human dietary exposure. Environ Sci Technol 41:2178–2183

    Article  CAS  PubMed  Google Scholar 

  • Williams PN, Villada A, Deacon C, Raab A, Figuerola J, Green AJ, Feldmann J, Meharg AA (2007b) Greatly enhanced arsenic shoot assimilation in rice leads to elevated grain levels compared to wheat and barley. Environ Sci Technol 41:6854–6859

    Article  CAS  PubMed  Google Scholar 

  • Wu ZC, Ren HY, McGrath SP, Wu P, Zhao FJ (2011) Investigating the contribution of the phosphate transport pathway to arsenic accumulation in rice. Plant Physiol 157:498–508

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xu H, Allard B, Grimvall A (1991) Effects of acidification and natural organic materials on the mobility of arsenic in the environment. Water Air Soil Pollut 57–8:269–278

    Article  Google Scholar 

  • Xu XY, McGrath SP, Meharg A, Zhao FJ (2008) Growing rice aerobically markedly decreases arsenic accumulation. Environ Sci Technol 42:5574–5579

    Article  CAS  PubMed  Google Scholar 

  • Ye WL, Wood BA, Stroud JL, Andralojc PJ, Raab A, McGrath SP, Feldmann J, Zhao FJ (2010) Arsenic speciation in phloem and xylem exudates of castor bean. Plant Physiol 154:1505–1513

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zavala YJ, Gerads R, Gürleyük H, Duxbury JM (2008) Arsenic in rice: II. Arsenic speciation in USA grain and implications for human health. Environ Sci Technol 42:3861–3866

    Article  CAS  PubMed  Google Scholar 

  • Zhao FJ, Harris E, Yan J, Ma JC, Wu LY, Liu WJ, McGrath SP, Zhou JZ, Zhu YG (2013a) Arsenic methylation in soils and its relationship with microbial arsM abundance and diversity, and As speciation in rice. Environ Sci Technol 47:7147–7154

    CAS  PubMed  Google Scholar 

  • Zhao FJ, McGrath SP, Meharg AA (2010) Arsenic as a food-chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies. Ann Rev Plant Biol 61:535–559

    Article  CAS  Google Scholar 

  • Zhao FJ, Zhu YG, Meharg AA (2013b) Methylated arsenic species in rice: Geographical variation, origin, and uptake mechanisms. Environ Sci Technol 47:3957–3966

    Article  CAS  PubMed  Google Scholar 

  • Zheng MZ, Cai C, Hu Y, Sun GX, Williams PN, Cui HJ, Li G, Zhao FJ, Zhu YG (2011) Spatial distribution of arsenic and temporal variation of its concentration in rice. New Phytol 189:200–209

    Article  CAS  PubMed  Google Scholar 

  • Zhu YG, Sun GX, Lei M, Teng M, Liu YX, Chen NC, Wang LH, Carey AM, Deacon C, Raab A, Meharg AA, Williams PN (2008) High percentage inorganic arsenic content of mining impacted and nonimpacted Chinese rice. Environ Sci Technol 42:5008–5013

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the Natural Science Foundation of China (41330853, 41073074), the Innovative Research Team Development Plan of the Ministry of Education of China (IRT1256) and a Rothamsted International fellowship. Rothamsted Research is supported by the UK Biotechnology and Biological Sciences Research Council. We thank Professor Jian Feng Ma of Okayama University for providing silica gel.

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Correspondence to Fang-Jie Zhao.

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Responsible Editor: Henk Schat.

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Liu, WJ., McGrath, S.P. & Zhao, FJ. Silicon has opposite effects on the accumulation of inorganic and methylated arsenic species in rice. Plant Soil 376, 423–431 (2014). https://doi.org/10.1007/s11104-013-1991-7

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  • DOI: https://doi.org/10.1007/s11104-013-1991-7

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