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Impact of Elevated Nitrate and Perchlorate in Irrigation Water on the Uptake, Speciation, and Accumulation of Arsenic in Rice (Oryza sativa L.)

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Abstract

In the absence of adequate molecular oxygen in a continuously flooded soil, other oxidizing anions can potentially oxidize arsenite (As(III)) into arsenate (As(V)) and reduce the bioavailability of arsenic (As) to rice while maintaining high rice yield. We conducted a greenhouse study to evaluate the effect of two prevalent oxyanions (10 mg/L nitrate and/or 50 μg/L perchlorate) on the As uptake, speciation, and accumulation in a hybrid rice (XL753) at the heading and maturity stages. The presence of nitrate and/or perchlorate at the used concentrations increased the rice grain yield by 35–93% to16.6–23.8 g/pot while lowering the total As in rice grains by 34–45% to 0.81–0.97 mg/kg dry weight. Perchlorate alone led to the greatest decrease in total As. Organic As was the predominant species in rice grains, with dimethylarsinic acid (DMA) accounting for 66–76% of total As in all treatments. In contrast, inorganic As was the dominant As form in rice straws and roots, with As(V) accounting for 62.4–91.4% of total As in all treatments. The translocation and accumulation of different As species in rice tissues varied at different growth stages in the presence of two tested oxyanions, as indicated by the ratios of inorganic vs organic As and inorganic As(III) vs As(V). Overall, the presence of oxyanions in irrigation water at the tested concentrations significantly decreased the total As accumulation in rice grains, while enhancing the rice yield.

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References

  • Blake, G. R., & Hartge, K. H. (1986). Bulk density. In A. Klute (Ed.), Methods of soil analysis. Part 1. 2nd ed. Agron. Monogr. 9 (pp. 363–375). Madison: ASA and SSSA.

    Google Scholar 

  • Carey, A. M., Scheckel, K. G., Lombi, E., Newville, M., Choi, Y., Norton, G. J., Charnock, J. M., Feldmann, J., Price, A. H., & Meharg, A. A. (2010). Grain unloading of arsenic species in rice. Plant Physiology, 152, 309–319.

    CAS  Google Scholar 

  • Carey, A. M., Norton, G. J., Deacon, C., Scheckel, K. G., Lombi, E., et al. (2011). Phloem transport of arsenic species from flag leaf to grain during grain filling. New Phytologist, 192, 87–98.

    CAS  Google Scholar 

  • Carlson, H. K., Kuehl, J. V., Hazra, A. B., Justice, N. B., Stoeva, M. K., Sczesnak, A., Mullan, M. R., Iavarone, A. T., Engelbrektson, A., Price, M. N., Deutschbauer, A. M., Arkin, A. P., & Coates, J. D. (2015). Mechanisms of direct inhibition of the respiratory sulfate-reduction pathway by (per) chlorate and nitrate. ISME Journal, 9(6), 1295–1305.

    CAS  Google Scholar 

  • Carrijo, D. R., Lundy, M. E., & Linquist, B. A. (2017). Rice yields and water use under alternate wetting and drying irrigation: a metal-analysis. Field Crop Research, 203, 173–180.

    Google Scholar 

  • Chen, G. K., Li, X. B., He, H. Z., Li, H. S., & Zhang, Z. M. (2015a). Varietal differences in the growth of rice seedling exposed to perchlorate and their antioxidative defense mechanisms. Environmental Toxicology Chemistry, 34(8), 1926–1933.

    CAS  Google Scholar 

  • Chen, G. K., He, H. Z., Gao, H. S., Li, H. S., & Zhang, Z. M. (2015b). Differential responses of two rice varieties to perchlorate stress. Polish Journal of Environmental Studies, 24(1), 67–74.

    CAS  Google Scholar 

  • Chen, Y. S., Han, Y. H., Cao, Y., Zhu, Y. G., Rathinasabapathi, B., & Ma, L. Q. (2017). Arsenic transport inrice and biological solutions to reduce arsenic risk from rice. Frontier in Plant Science., 8, 268.

    Google Scholar 

  • Chiang, H. C., & Tsou, T. C. (2009). Arsenite enhances the benzo [a] pyrene diol epoxide (BPDE)-induced mutagenesis with no marked effect on repair of BPDE-DNA adducts in human lung cells. Toxicology In Vitro, 23(5), 897–905.

    CAS  Google Scholar 

  • Davidson, E.A., David, M.B., Galloway, J.N., Goodale, C.L., Haeuber, R., Harrison, J.A., Howarth, R.W., Jaynes, D.B., Lowrance, R.R., Nolan, B.T., Peel, J.L., Pinder, R.W., Porter, E., Snyder, C.S., Townsend, A.R., Ward, M.H. (2012). Excess nitrogen in the U.S. environment: trends, risks, and solutions. Issues in Ecology, Report Number 15, Winter 2012.

  • Dixit, S., & Hering, J. G. (2003). Comparison of arsenic(V) and arsenic (III) sorption onto iron oxide minerals: implications for arsenic mobility. Environmental Science & Technology, 37(18), 4182–4189.

    CAS  Google Scholar 

  • Dou, F., & Tarpley, L. (2014). 2012 Variety evaluation for main crop yield potential. In M. O. Way, G. N. McCauley, S. Zhou, L. T. Wilson, & B. Morace (Eds.), Texas rice production guidelines (Vol. B-6131, pp. 24–26). Texas A&M AgriLife Extension and Texas A&M AgriLife Research.

  • Dou, F., Wright, A. L., & Hons, F. M. (2008). Dissolved and soil organic C after long-term conventional and no-till sorghum cropping. Communications in Soil Science and Plant Analysis, 39, 667–679.

    CAS  Google Scholar 

  • Duan, Y. H., Zhang, Y. L., Ye, L. T., Fan, X. R., Xu, G. H., & Shen, Q. R. (2007). Response of rice cultivars with different nitrogen use efficiency to partial nitrate nutrition. Annals of Botany, 99, 1153–1160.

    CAS  Google Scholar 

  • Dubrovsky, N.M., Burow, K.R., Clark, G.M., Gronberg, J.M., Hamilton, P.A., Hitt, K.J., Mueller, D.K., Munn, M.D., Nolan, B.T., Puckett, L.J., Rupert, M.G., Short, T.M., Spahr, N.E., Sprague, L.A., Wilber, W.G. (2010). Nutrients in the nation’s streams and groundwater, 1992–2004. USGS Circular 1350, United States Geological Survey.

  • Gilbert-Diamond, D., Cottingham, K.L., Gruber, J.F., Punshon, T., Sayarath, V., Gandolfi, A.J., Baker, E.R., Jackson, B.P., Folt, C.L., Karagas, M.R. (2011). Rice consumption contributes to arsenic exposure in US women. Proceedings of National Academy of Science of USA (PNAS), 108, 20656-20660.

  • Gurdak, J. J., & Qi, S. L. (2012). Vulnerability of recently recharged groundwater in principle aquifers of the United States to nitrate contamination. Environmental Science & Technology, 46(11), 6004–6012.

    CAS  Google Scholar 

  • Harter, T., Dzurella, K., Kourakos, G., Hollander, A., Bell, A., Santos, N., Hart, Q., King, A., Quinn, J., Lampinen, G., Liptzin, D., Rosenstock, T., Zhang, M., Pettygrove, G.S., Tomich, T. (2017). Nitrogen fertilizer loading to groundwater in the Central Valley. Final report to the fertilizer research education program, Projects 11-0301 and 15-0454, California Department of Food and Agriculture and University of California Davis, 325p.

  • Hu, M., Li, F., Liu, C., & Wu, W. (2015). The diversity and abundance of As (III) oxidizers on root iron plaque is critical for arsenic bioavailability to rice. Scientific Reports, 5, 13611.

    Google Scholar 

  • ITRC (Interstate Technology & Regulatory Council). (2005). Perchlorate: overview of issues, status, and remedial options. PERCHLORATE-1. Washington, D.C.: Interstate Technology & Regulatory Council, Perchlorate Team. Available on the internet at http://www.itrcweb.org. Accessed 1 Dec 2019.

  • Jackson, A., Anandam, S. K., Anderson, T., Lehman, T., Rainwater, K., Rajagopalan, S., Ridley, M., & Tock, R. (2005). Perchlorate occurrence in the Texas southern high plains aquifer system. Ground Water Monitoring and Remediation, 25(1), 137–149.

    CAS  Google Scholar 

  • Jackson, W. A., Bohlke, J. K., Andraski, B. J., Fahlquist, L., Bexfield, L., Echardt, F. D., Gates, J. B., Davila, A. F., Mckay, C. P., Rao, B., Sevanthi, R., Rajagopalan, S., Estrada, N., Sturchio, N., Hatzinger, P. B., Anderson, T. A., Orris, G., Betancout, J., Stonestrom, D., Latorre, C., Li, Y., & Harvey, G. J. (2015). Global patterns and environmental controls of perchlorate and nitrate co-occurrence in arid and semi-arid environments. Geochimica et Cosmochimica Acta, 164, 502–522.

    CAS  Google Scholar 

  • Jia, Y., Huang, H., Chen, Z., & Zhu, Y. G. (2014). Arsenic uptake by rice is influenced by microbe-mediated arsenic redox changes in the rhizosphere. Environmental Science & Technology, 48(2), 1001–1007.

    CAS  Google Scholar 

  • Khan, M. A., Stroud, I. E., Zhu, Y. G., Mcgrath, S. P., & Zhao, F. J. (2010). Arsenic bioavailability to rice is elevated in Bangladeshi paddy soils. Environmental Science & Technology, 44, 8515–8521.

    CAS  Google Scholar 

  • Lin, Z. J., Wang, X., Wu, X., Liu, D. H., Yin, Y. L., Zhang, Y., Xiao, S., & Xing, B. S. (2018). Nitrate reduced arsenic redox transformation and transfer in flooded paddy soil-rice system. Environmental Pollution, 243, 1015–1025.

    CAS  Google Scholar 

  • Linquist, B. A., Anders, M. M., Adviento-Borbe, M. A., Chaney, R. L., Nalley, L. L., Da Rosa, E. F., & van Kessel, C. (2015). Reducing greenhouse gas emissions, water use, and grain arsenic levels in rice systems. Global Change Biology, 21, 407–417.

    Google Scholar 

  • Liu, W. J., Zhu, Y. G., Hu, Y., Williams, P. N., Gault, A. G., Meharg, A. A., Charnock, J. M., & Smith, F. A. (2006). Arsenic sequestration in iron plaque, its accumulation and speciation in mature rice plants (Oryza sativa L.). Environmental Science & Technology, 40, 5730–5736.

    CAS  Google Scholar 

  • Ma, J. F., Yamaji, N., Mitani, N., Xu, X. Y., Sy, Y. H., McGrath, S. P., & Zhao, F. J. (2008). Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proceedings of National Academy of Science of USA (PNAS), 105, 9931–9935.

    CAS  Google Scholar 

  • Nalley, L., Linquist, B., Kovacs, K., & Anders, M. (2015). The economic viability of alternative wetting and drying irrigation in Arkansas rice production. Agronomy Journal, 107, 579–587.

    Google Scholar 

  • Nolan, B. T., & Hitt, K. J. (2006). Vulnerability of shallow groundwater and drinking-water wells to nitrate in the United States. Environmental Science & Technology, 40(24), 7834–7840.

    CAS  Google Scholar 

  • Norton, G. J., Douglas, A., Lahner, B., Yakubova, E., Guerinot, M. L., et al. (2014). Genome wide association mapping of grain arsenic, copper, molybdenum and zinc in rice (Oryza sativa L.) grown at four international field sites. PLoS One, 9(2), e89685.

    Google Scholar 

  • Oremland, R. S., & Stolz, J. F. (2003). The ecology of arsenic. Science, 300(5621), 939–944.

    CAS  Google Scholar 

  • Oremland, R. S., & Stolz, J. F. (2005). Arsenic, microbes and contaminated aquifers. Trends in Microbiology, 13(2), 45–49.

    CAS  Google Scholar 

  • Pinson, S. R., Tarpley, L., Yan, W., Yeater, K., Lahner, B., Yakubova, E., Huang, X. Y., Zhang, M., Guerinot, M. L., & Salt, D. E. (2015). Worldwide genetic diversity for mineral element concentrations in rice grain. Crop Science, 55, 294–311.

    CAS  Google Scholar 

  • Pushon, T., Jackson, B. P., Meharg, A. A., Warczark, T., Scheckel, K., & Guerinot, M. L. (2017). Understanding arsenic dynamics in agronomic systems to predict and prevent uptake by crop plants. Science of the Total Environment, 581-582, 209–220.

    Google Scholar 

  • Rahman, M. A., Hasegawa, H., Rahman, M. M., Rahman, M. A., & Miah, M. A. M. (2007). Accumulation of arsenic in tissues of rice plant (Oryza sativa L.) and its distribution in fractions of rice grain. Chemosphere, 69, 942–948.

    CAS  Google Scholar 

  • Rhoades, J. D. (1982). Soluble salts. In A. L. Page et al. (Eds.), Methods of soil analysis: part 2. Agronomy Monogr. 9 (2nd ed., pp. 167–178). Madison: ASA and SSSA.

    Google Scholar 

  • Ringuet, S., Sassano, L., & Johnson, Z. I. (2011). A suite of microplate reader-based colorimetric methods to quantify ammonium, nitrate, orthophosphate and silicate concentrations for aquatic nutrient monitoring. Journal of Environmental Monitoring, 13, 370–376.

    CAS  Google Scholar 

  • Sanchez, C. A., Krieger, R. I., Khandaker, R. N., Moore, R. C., Holts, K. C., & Neidel, L. L. (2005). Accumulation and perchlorate exposure potential of lettuce produced in the lower Colorado River region. Journal of Agricultural and Food Chemistry, 53(13), 5479–5486.

    CAS  Google Scholar 

  • Schofield, R. K., & Taylor, A. W. (1955). The measurement of soil pH. Soil Science Society of America Proceedings., 19, 164–167.

    CAS  Google Scholar 

  • Shi, S., Wang, T., Chen, Z., Tang, Z., Wu, Z., Salt, D. E., et al. (2016). OsHAC1;1 and OsHAC1;2 function as arsenate reductases and regulate arsenic accumulation. Plant Physiologist, 172, 1708–1719.

    CAS  Google Scholar 

  • Shri, M., Singh, P. K., Kidwai, M., Gautum, N., Dubey, S., Verma, G., & Chakrabarty, D. (2019). Recent advances in arsenic metabolism in plants: current status, challenges and highlighted biotechnological intervention to reduce grain arsenic in rice. Metallomics, 11, 519–532.

    CAS  Google Scholar 

  • Singh, N., Kumar, D., & Sahu, A. P. (2007). Arsenic in the environment: effects on human health and possible prevention. Journal of Environmental Biology, 28, 359–365.

    CAS  Google Scholar 

  • Song, W. Y., Yamaki, T., Yamaji, N., Ko, D., Jung, K. H., Fujii-Kashino, M., An, G., Martinoia, E., Lee, Y., & Ma, J. F. (2014). A rice ABC transporter, OsABCC1, reduces arsenic accumulation in the grain. Proceedings of National Academy of Science of USA (PNAS), 111, 15699–15704.

    CAS  Google Scholar 

  • Sowers, T. D., Harrington, J. M., Polizzotto, M. L., & Duckworth, O. W. (2017). Sorption of arsenic to biogenic iron (oxyhydr)oxides produced in circumneutral environments. Geochimica et Cosmochimica Acta, 198, 194–207.

    CAS  Google Scholar 

  • Su, Y., McGrath, S. P., & Zhao, F. J. (2010). Rice is more efficient in arsenite uptake and translocation than wheat and barley. Plant and Soil, 328, 27–34.

    CAS  Google Scholar 

  • Sun, W. J., Sierra-Alvarez, R., Fernandez, N., Sanz, J. L., Amils, R., Legatzki, A., Maier, R. M., & Field, J. A. (2009a). Molecular characterization and in situ quantification of anoxic arsenite-oxidizing denitrifying enrichment cultures. FEMS Microbiology Ecology, 68(1), 72–85.

    CAS  Google Scholar 

  • Sun, W. J., Sierra-Alvarez, R., Milner, L., Oremland, R., & Field, J. A. (2009b). Arsenite and ferrous iron oxidation linked to chemolithotrophic denitrification for the immobilization of arsenic in anoxic environments. Environmental Science & Technology, 43(17), 6585–6591.

    CAS  Google Scholar 

  • Sun, W. J., Sierra-Alvarez, R., Milner, L., & Field, J. A. (2010). Anaerobic oxidation of arsenite linked to chlorate reduction. Applied and Environmental Microbiology, 76(20), 6804–6811.

    CAS  Google Scholar 

  • Suriyagoda, L. D. B., Dittert, K., & Lambers, H. (2018). Mechanism of arsenic uptake, translocation and plant resistance to accumulate arsenic in rice grains. Agriculture Ecosystems & Environment, 253, 23–37.

    CAS  Google Scholar 

  • U.S. Food and Drug Administration (U.S. FDA). (2013). Arsenic in rice: full analytical result from rice/rice product sampling. September. U.S. FDA, Silver Spring, MD, USA.

  • Van Metre, P. C., Frey, J. W., Musgrove, M., Nakagaki, N., Qi, S., Mahler, B. J., Wieczorek, M. E., & Button, D. T. (2016). High nitrate concentrations in some Midwest United States streams in 2013 after the 2012 drought. Journal of Environmental Quality, 45(5), 1696–1704.

    Google Scholar 

  • Wang, X. Q., Liu, T. X., Li, F. B., Li, B., & Liu, C. P. (2018a). Effects of simultaneous application of ferrous iron and nitrate on arsenic accumulation in rice grown in contaminated paddy soil. ACS Earth Space Chemistry, 2(2), 103–111.

    CAS  Google Scholar 

  • Wang, X. X., Sun, W. J., Zhang, S., Sharifan, H., & Ma, X. M. (2018b). Elucidating the effects of cerium oxide nanoparticles and zinc oxide nanoparticles on arsenic uptake and speciation in rice (Oryza sativa) in a hydroponic system. Environmental Science & Technology, 52(17), 10040–10047.

    CAS  Google Scholar 

  • Xie, Y. F., Tao, G. S., Chen, Q., & Tian, X. Y. (2014). Effects of perchlorate stress on growth and physiological characteristics of Rice (Oryza sativa L.) seedlings. Water, Air & Soil Pollution, 225, 2077.

    Google Scholar 

  • Xu, X. Y., MaGrath, S. P., Meharg, A. A., & Zhao, F. J. (2008). Growing rice aerobically markedly decreases arsenic accumulation. Environmental Science & Technology, 42, 5574–5579.

    CAS  Google Scholar 

  • Ye, W. L., Wood, B. A., Stroud, J. L., Andralojc, P. J., Raab, A., McGrath, S. P., Feldmann, J., & Zhao, F. J. (2010). Arsenic speciation in phloem and xylem exudates of castor bean. Plant Physiologist, 154, 1505–1513.

    CAS  Google Scholar 

  • Zhang, J., Zhao, S., Xu, Y., Zhou, W., Huang, K., Tang, Z., et al. (2017). Nitrate stimulates anaerobic microbial arsenite oxidation in paddy soils. Environmental Science & Technology, 51, 4377–4386.

    CAS  Google Scholar 

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Ma, X., Sun, K.Y., Dou, F. et al. Impact of Elevated Nitrate and Perchlorate in Irrigation Water on the Uptake, Speciation, and Accumulation of Arsenic in Rice (Oryza sativa L.). Water Air Soil Pollut 231, 309 (2020). https://doi.org/10.1007/s11270-020-04701-z

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