Skip to main content
Log in

Distribution and accumulation of mercury in pot-grown African rice cultivars (Oryza glaberrima Steud. and Oryza sativa L.) determined via LA-ICP-MS

  • Original Paper
  • Published:
Environmental Geochemistry and Health Aims and scope Submit manuscript

Abstract

There is limited information concerning the distribution of mercury in rice, particularly in African rice. The objective was to compare the distribution of total mercury (THg) and methylmercury (MeHg) in African rice (Oryza glaberrima Steud.) and Asian rice (O. sativa L.). It is hypothesized that increased mineral accumulation and greater stress tolerance in O. glaberrima will affect the uptake and distribution of THg and MeHg, compared to O. sativa. Rice varieties from the Republic of Mali, including O. glaberrima (n =1) and O. sativa (n = 2), were cultivated in a greenhouse, in mercury-spiked soil (50 mg/kg) (n =3 replicates/variety). THg and MeHg concentrations were analyzed in the grain (brown rice), and the THg distribution was analyzed using laser ablation inductively coupled-plasma mass spectrometry (LA-ICP-MS). THg and MeHg concentrations did not differ between O. glaberrima and O. sativa grain. However, in both O. sativa varieties, THg was highly concentrated in the scutellum, which surrounds the embryo and is removed during polishing. Conversely, in O. glaberrima grain, THg was widely distributed throughout the endosperm, the edible portion of the grain. Differences in the THg distribution in O. glaberrima grain, compared to O. sativa, may elevate the risk of mercury exposure through ingestion of polished rice. The novelty of this study includes the investigation of a less-studied rice species (O. glaberrima), the use of a highly sensitive elemental imaging technique (LA-ICP-MS), and its finding of a different grain THg distribution in O. glaberrima than has been observed in O. sativa.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Ballatori, N. (2002). Transport of toxic metals by molecular mimicry. Environmental Health Perspectives, 110, 689–694. https://doi.org/10.1289/ehp.02110s5689

    Article  CAS  Google Scholar 

  • Carey, A. M., Norton, G. J., Deacon, C., Scheckel, K. G., Lombi, E., Punshon, T., Guerinot, M. L., Lanzirotti, A., Newville, M., Choi, Y., Price, A. H., & Meharg, A. A. (2011). Phloem transport of arsenic species from flag leaf to grain during grain filling. New Phytologist, 192, 87–98. https://doi.org/10.1111/j.1469-8137.2011.03789.x

    Article  CAS  Google Scholar 

  • Food and Agriculture Organization of the United Nations (FAO) (2021). FAOSTAT. Retrieved June 13, 2021, from http://www.fao.org/faostat/en/#data.

  • Futakuchi, K., Sie, M., & Saito, K. (2012). Yield potential and physiological and morphological characteristics related to yield performance in Oryza glaberrima Steud. Plant Production Science, 15, 151–163. https://doi.org/10.1626/pps.15.151

    Article  Google Scholar 

  • Gerson, J. R., Driscoll, C. T., Hsu-Kim, H., & Bernhardt, E. S. (2018). Senegalese artisanal gold mining leads to elevated total mercury and methylmercury concentrations in soils, sediments, and rivers. Elementa Science of the Anthropocene. https://doi.org/10.1525/elementa.274

    Article  Google Scholar 

  • Gibb, H., & O’Leary, K. G. (2014). Mercury exposure and health impacts among individuals in the artisanal and small-scale gold mining community: A comprehensive review. Environmental Health Perspectives, 122, 667–672. https://doi.org/10.1289/ehp.1307864

    Article  CAS  Google Scholar 

  • Hong, C., Yu, X., Liu, J., Cheng, Y., & Rothenberg, S. E. (2016). Low-level methylmercury exposure through rice ingestion in a cohort of pregnant mothers in rural China. Environmental Research, 150, 519–527. https://doi.org/10.1016/j.envres.2016.06.038

    Article  CAS  Google Scholar 

  • Jackson, B. P., Taylor, V. F., Karagas, M. R., Punshon, T., & Cottingham, K. L. (2012). Arsenic, organic foods, and brown rice syrup. Environmental Health Perspective, 120, 623–626. https://doi.org/10.1289/ehp.1104619

    Article  CAS  Google Scholar 

  • Jo, G., & Todorov, T. I. (2019). Distribution of nutrient and toxic elements in brown and polished rice. Food Chemistry, 289, 299–307. https://doi.org/10.1016/j.foodchem.2019.03.040

    Article  CAS  Google Scholar 

  • Jones, M. P., Dingkuhn, M., Aluko, G. K., & Semon, M. (1997). Interspecific Oryza Sativa L. X O. Glaberrima Steud. progenies in upland rice improvement. Euphytica, 92, 237–246.

    Article  Google Scholar 

  • Jones, M. P., Mande, S., & Aluko, K. (1997). Diversity and potential of Oryza glaberrima Steud in upland rice breeding. Breeding Science, 47, 395–398. https://doi.org/10.1270/jsbbs1951.47.395

    Article  CAS  Google Scholar 

  • Kopittke, P. M., Punshon, T., Paterson, D. J., Tappero, R. V., Wang, P., Blamey, F. P. C., van der Ent, A., & Lombi, E. (2018). Imaging of elements in plants using synchrotron-based X-ray fluorescence microscopy. Plant Physiology, 178, 507–523. https://doi.org/10.1104/pp.18.00759

    Article  CAS  Google Scholar 

  • Krishnan, S., & Dayanandan, P. (2003). Structural and histochemical studies on grain-filling in the caryopsis of rice (Oryza sativa L.). Journal of Biosciences, 28, 455–469.

    Article  CAS  Google Scholar 

  • Krishnan, S., Ebenezer, G. A. I., & Dayanandan, P. (2001). Histochemical localization of storage components in caryopsis of rice (Oryza sativa L.). Current Science, 80, 567–571.

    CAS  Google Scholar 

  • Li, Y., Hu, W., Zhao, J., Chen, Q., Wang, W., Li, B., & Li, Y.-F. (2019). Selenium decreases methylmercury and increases nutritional elements in rice growing in mercury-contaminated farmland. Ecotoxicology and Environmental Safety. https://doi.org/10.1016/j.ecoenv.2019.109447

    Article  Google Scholar 

  • Li, Y., Zhao, J., Zhang, B., Liu, Y., Xu, X., Li, Y.-F., Gao, Y., & Chai, Z. (2016). The influence of iron plaque on the absorption, translocation and transformation of mercury in rice (Oryza sativa L.) seedlings exposed to different mercury species. Plant and Soil, 398, 87–97. https://doi.org/10.1007/s11104-015-2627-x

    Article  CAS  Google Scholar 

  • Liang, L., Horvat, M., Cernichiari, E., Gelcin, B., & Balogh, S. (1996). Simple solvent extraction technique for elimination of matrix interferences in the determination of methylmercury in environmental and biological samples by ethylation-gas chromatography-cold vapor atomic fluorescence spectrometry. Talanta, 43, 1883–1888. https://doi.org/10.1016/0039-9140(96)01964-9

    Article  CAS  Google Scholar 

  • Linares, O. F. (2002). African rice (Oryza glaberrima): history and future potential. Proceedings of the National Academy of Sciences, 99, 16360–16365. https://doi.org/10.1073/pnas.252604599

    Article  CAS  Google Scholar 

  • Lindberg, S. E., Dong, W., Chanton, J., Qualls, R. G., & Meyers, T. (2005). A mechanism for bimodal emission of gaseous mercury from aquatic macrophytes. Atmospheric Environment, 39, 1289–1301. https://doi.org/10.1016/j.atmosenv.2004.11.006

    Article  CAS  Google Scholar 

  • Lombi, E., de Jonge, M. D., Donner, E., Kopittke, P. M., Howard, D. L., Kirkham, R., Ryan, C. G., & Paterson, D. (2011). Fast X-ray fluorescence microtomography of hydrated biological samples. Plos One. https://doi.org/10.1371/journal.pone.0020626

    Article  Google Scholar 

  • Lombi, E., Scheckel, K. G., Pallon, J., Carey, A. M., Zhu, Y. G., & Meharg, A. A. (2009). Speciation and distribution of arsenic and localization of nutrients in rice grains. New Phytologist, 189, 193–201. https://doi.org/10.1111/j.1469-8137.2009.02912.x

    Article  CAS  Google Scholar 

  • Majerus, V., Bertin, P., & Lutts, S. (2007). Effects of iron toxicity on osmotic potential, osmolytes and polyamines concentrations in the African rice (Oryza glaberrima Steud.). Plant Science, 173, 96–105. https://doi.org/10.1016/j.plantsci.2007.04.003

    Article  CAS  Google Scholar 

  • Majerus, V., Bertin, P., & Lutts, S. (2009). Abscisic acid and oxidative stress implications in overall ferritin synthesis by African rice (Oryza glaberrima Steud.) seedlings exposed to short term iron toxicity. Plant and Soil, 324, 253–265. https://doi.org/10.1007/s11104-009-9952-x

    Article  CAS  Google Scholar 

  • Mason, R. P., Baumann, Z., Hansen, G., Yao, K. M., Coulibaly, M., & Coulibaly, S. (2019). An assessment of the impact of artisanal and commercial gold mining on mercury and methylmercury levels in the environment and fish in Cote d’Ivoire. Science of the Total Environment, 665, 1158–1167. https://doi.org/10.1016/j.scitotenv.2019.01.393

    Article  CAS  Google Scholar 

  • Meharg, A. A., Lombi, E., Williams, P. N., Scheckel, K. G., Feldmann, J., Raab, A., Zhu, Y., & Islam, R. (2008). Speciation and localization of arsenic in white and brown rice grains. Environmental Science & Technology, 42, 1051–1057. https://doi.org/10.1021/es702212p

    Article  CAS  Google Scholar 

  • Meng, B., Feng, X., Qiu, G., Anderson, C. W. N., Wang, J., & Zhao, L. (2014). Localization and speciation of mercury in brown rice with implications for pan-Asian public health. Environmental Science & Technology, 48, 7974–7981. https://doi.org/10.1021/es502000d

    Article  CAS  Google Scholar 

  • National Research Council (NRC) (2000). Toxicological Effects of Methylmercury. National Academy Press.

  • Ohmori, Y., Sotta, N., & Fujiwara, T. (2016). Identification of introgression lines of Oryza glaberrima Steud. with high mineral content in grains. Journal of Soil Science & Plant Nutrition, 62, 456–464. https://doi.org/10.1080/00380768.2016.1204896

    Article  CAS  Google Scholar 

  • Park, J., Song, W. Y., Ko, D., Eom, Y., Hansen, T. H., Schiller, M., Lee, T. G., Martinoia, E., & Lee, Y. (2012). The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant Journal, 69, 278–88. https://doi.org/10.1111/j.1365-313X.2011.04789.x

    Article  CAS  Google Scholar 

  • Global Rice Science Partnership (GRiSP) (2013). Rice almanac, 4th edition. International Rice Research Institute.

  • Pushie, M. J., Pickering, I. J., Korbas, M., Hackett, M. J., & George, G. N. (2014). Elemental and chemically specific x-ray fluorescence imaging of biological systems. Chemical Reviews, 114, 8499–8541. https://doi.org/10.1021/cr4007297

    Article  CAS  Google Scholar 

  • Qiu, G., Feng, X., Li, P., Wang, S., Li, G., Shang, L., & Fu, X. (2008). Methylmercury accumulation in rice (Oryza sativa L.) grown at abandoned mercury mines in Guizhou, China. Journal of Agricultural and Food Chemistry, 56, 2465–2468. https://doi.org/10.1021/jf073391a

    Article  CAS  Google Scholar 

  • Rothenberg, S. E., Feng, X., Zhou, W., Tu, M., Jin, B., & You, J. (2012). Environment and genotype controls on mercury accumulation in rice (Oryza sativa L.) cultivated along a contamination gradient in Guizhou China. Science of the Total Environment, 426, 272–280. https://doi.org/10.1016/j.scitotenv.2012.03.024

    Article  CAS  Google Scholar 

  • Rothenberg, S. E., Mgutshini, N. L., Bizimis, M., Johnson-Beebout, S. E., & Ramanantsoanirina, A. (2015). Retrospective study of methylmercury and other metal(loid)s in Madagascar unpolished rice (Oryza sativa L.). Environmental Pollution, 196, 125–133. https://doi.org/10.1016/j.envpol.2014.10.002

    Article  CAS  Google Scholar 

  • Rothenberg, S. E., Windham-Myers, L., & Creswell, J. E. (2014). Rice methylmercury exposure and mitigation: A comprehensive review. Environmental Research, 133, 407–423. https://doi.org/10.1016/j.envres.2014.03.001

    Article  CAS  Google Scholar 

  • Schwesig, D., & Krebs, O. (2003). The role of ground vegetation in the uptake of mercury and methylmercury in a forest ecosystem. Plant and Soil, 253, 445–455. https://doi.org/10.1023/A:1024891014028

    Article  CAS  Google Scholar 

  • Semon, M., Nielsen, R., Jones, M. P., & McCouch, S. R. (2005). The population structure of African cultivated rice Oryza glaberrima (Steud.): evidence for elevated levels of LD caused by admixture with O. sativa and ecological adaptation. Genetics, 169, 1639–1647. https://doi.org/10.1534/genetics.104.033175

    Article  CAS  Google Scholar 

  • Song, W.-Y., Park, J., Mendoza-Cózatl, D. G., Suter-Grotemeyer, M., Shim, D., Hörtensteiner, S., Geisler, M., Weder, B., Rea, P. A., Rentsch, D., Schroeder, J. I., Lee, Y., & Martnoia, E. (2010). Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proceedings of the National Academy of Sciences of the United States of America, 107, 21187–21192. https://doi.org/10.1073/pnas.1013964107

    Article  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 the National Academy of Sciences of the United States of America, 111, 15699–15704. https://doi.org/10.1073/pnas.1414968111

    Article  CAS  Google Scholar 

  • Strickman, R. J., & Mitchell, C. P. J. (2017). Accumulation and translocation of methylmercury and inorganic mercury in Oryza sativa: An enriched isotope tracer study. Science of the Total Environment, 574, 1415–1423. https://doi.org/10.1016/j.scitotenv.2016.08.068

    Article  CAS  Google Scholar 

  • Sweeney, M., & McCouch, S. (2007). The complex history of the domestication of rice. Annals of Botany, 100, 951–957. https://doi.org/10.1093/aob/mcm128

    Article  Google Scholar 

  • U.S. Environmental Protection Agency (U.S. EPA) (1998). Method 6020a, Inductively Coupled Plasma-Mass Spectrometry.

  • U.S. Environmental Protection Agency (U.S. EPA) (2001). Method 1630, Methyl Mercury in Water by Distillation, Aqueous Ethylation, Purge and Trap, and Cold Vapor Atomic Spectrometry.

  • U.S. Environmental Protection Agency (U.S. EPA) (2007a). Method 7473, Mercury in Solids and Solutions by Thermal Decomposition Amalgamation, and Atomic Absorption Spectrophotometry.

  • U.S. Environmental Protection Agency (U.S. EPA) (2007b). Method 3051A, Microwave Assisted Acid Digestion of Sediments, Sludges, Soils, and Oils.

  • VanderSchee, C. R., Kuter, D., Chou, H., Jackson, B. P., Mann, K. K., & Bohle, D. S. (2020). Addressing K/L-edge overlap in elemental analysis from micro-X-ray fluorescence: Bioimaging of tungsten and zinc in bone tissue using synchrotron radiation and laser ablation inductively coupled plasma mass spectrometry. Analytical and Bioanalytical Chemistry, 412, 259–265. https://doi.org/10.1007/s00216-019-02244-9

    Article  CAS  Google Scholar 

  • Villareal, C. P., Maranville, J. W., & Juliano, B. O. (1991). Nutrient content and retention during milling of brown rices from the International Rice Research Institute. Cereal Chemistry, 68, 437–439.

    CAS  Google Scholar 

  • Wang, Y., Habibullah-Al-Mamun, M., Han, J., Wang, L., Zhu, Y., Xu, X., Li, N., & Qiu, G. (2020). Total mercury and methylmercury in rice: exposure and health implications in Bangladesh. Environmental Pollution 265 (Part A), 114991. https://doi.org/10.1016/j.envpol.2020.114991.

  • Windham, L., Weis, J. S., & Weis, P. (2001). Patterns and processes of mercury release from leaves of two dominant salt marsh macrophytes, Phragmites australis and Spartina alterniflora. Estuaries, 24, 787–795. https://doi.org/10.2307/1353170

    Article  Google Scholar 

  • Wopereis, M. C. S., Johnson, D., Ahmadi, N., Tollens, E., & Jalloh, A. (2013). Realizing Africa’s Rice Promise. CAB International.

    Book  Google Scholar 

  • Xu, Xiaochang, Han, J., Abeysinghe, K. S., Atapattu, A. J., De Silva, P. M. C. S., Xu, Z., Long, S., & Qiu, G. (2020). Dietary exposure assessment of total mercury and methylmercury in commercial rice in Sri Lanka. Chemosphere, 239, 124749. https://doi.org/10.1016/j.chemosphere.2019.124749

    Article  CAS  Google Scholar 

  • Xu, Xiaohan, Zhao, J., Li, Y., Fan, Y., Zhu, N., Gao, Y., Li, B., Liu, H., & Li, Y.-F. (2016). Demethylation of methylmercury in growing rice plants: an evidence of self-detoxification. Environmental Pollution, 210, 113–120. https://doi.org/10.1016/j.envpol.2015.12.013

    Article  CAS  Google Scholar 

  • Yin, R., Feng, X., & Meng, B. (2013). Stable mercury isotope variation in rice plants (Oryza sativa L.) from the Wanshan mercury mining district SW China. Environmental Science & Technology, 47, 2238–2245. https://doi.org/10.1021/es304302a

    Article  CAS  Google Scholar 

Download references

Funding

TP, BJ, and the Dartmouth Trace Element Analysis Core were funded in part by the US National Institute of Environmental Health Sciences (grant number P42 ES007373). BJ was funded in part by the US National Cancer Institute (Cancer Center Support Grant, number 5P30 CA023108-41).

Author information

Authors and Affiliations

Authors

Contributions

SR, TP, and BJ designed and conceived of the study, acquired and analyzed the data, and wrote and revised the manuscript. AD and CH assisted with data collection. All authors reviewed and approved the manuscript.

Corresponding author

Correspondence to Sarah E. Rothenberg.

Ethics declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Ethics Approval

This research does not involve human participants and/or animals, and no ethical approval is required.

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1147 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Punshon, T., Jackson, B.P., Donohue, A. et al. Distribution and accumulation of mercury in pot-grown African rice cultivars (Oryza glaberrima Steud. and Oryza sativa L.) determined via LA-ICP-MS. Environ Geochem Health 44, 4077–4089 (2022). https://doi.org/10.1007/s10653-021-01169-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10653-021-01169-6

Keywords

Navigation