Skip to main content
SpringerLink
Log in

Effects of environment and genotype on mercury and methylmercury accumulation in rice (Oryza sativa L.)

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Rice grains contaminated by mercury (Hg) and methylmercury (MeHg) pose risks to human health. This study evaluated the relative importance of genotype, environment and genotype-environment interactions on the accumulation of total Hg (THg) and MeHg in brown rice.

Methods

A pot trial with four rice genotypes and 10 Hg-contaminated paddy soils was conducted under greenhouse conditions. The effects of genotype, environment and genotype-environment interactions on brown rice THg and MeHg accumulation were assessed by an Additive Main Effects and Multiplicative Interaction (AMMI) model.

Results

THg and MeHg concentrations in brown rice ranged from 20.5 to 75.5 μg kg−1 and 2.24 to 54.7 μg kg−1, respectively. The AMMI model indicated that genotype explained 41.1 and 19.6%, environment described 40.6 and 55.8%, and the genotype-environment interaction explained 11.9 and 20.0% of the variation in brown rice THg and MeHg levels, respectively. Brown rice THg positively correlated with water-soluble Hg and total potassium, but negatively correlated with total sulphur, iron, total organic carbon and nickel in soils. Brown rice MeHg negatively correlated with soil pH and selenium.

Conclusion

THg accumulation in brown rice was mainly affected by both genotype and environment, whereas MeHg accumulation was largely determined by environment.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ahmed ZU, Panaullah GM, Gauch H, McCouch SR, Tyagi W, Kabir MS, Duxbury JM (2011) Genotype and environment effects on rice (Oryza sativa L.) grain arsenic concentration in Bangladesh. Plant Soil 338:367–382

    Article  CAS  Google Scholar 

  • Barnett MO, Harris LA, Turner RR, Stevenson RJ, Henson TJ, Melton RC, Hoffman DP (1997) Formation of mercuric sulfide in soil. Environ Sci Technol 31:3037–3043

    Article  CAS  Google Scholar 

  • Bloom NS, Preus E, Katon J, Hiltner M (2003) Selective extractions to assess the biogeochemically relevant fractionation of inorganic mercury in sediments and soils. Anal Chim Acta 479:233–248

    Article  CAS  Google Scholar 

  • Corrales J, Naja GM, Dziuba C, Rivero RG, Orem W (2011) Sulfate threshold target to control methylmercury levels in wetland ecosystems. Sci Total Environ 409(11):2156–2162

    Article  PubMed  CAS  Google Scholar 

  • De Mendiburu F (2016) Agricolae: Statistical procedures for agricultural research. R package version 1:2–4 https://CRAN.R-project.org/package=agricolae

    Google Scholar 

  • Ding CF, Zhang TL, Li XG, Wang XX (2014) Major controlling factors and prediction models for mercury transfer from soil to carrot. J Soil Sediment 14:1136–1146

    Article  CAS  Google Scholar 

  • Fairbrother A, Wenstel R, Sappington K, Wood W (2007) Framework for metals risk assessment. Ecotox Environ Safe 68:145–227

    Article  CAS  Google Scholar 

  • Feng XB, Li P, Qiu GL, Wang S, Li GH, Shang LH, Meng B, Jiang HM, Bai WY, Li ZG, Fu XW (2008) Human exposure to methylmercury through rice intake in mercury mining areas, Guizhou Province, China. Environ Sci Technol 42:326–332

    Article  PubMed  CAS  Google Scholar 

  • Feng C, Pedrero Z, Li P, Du B, Feng XB, Monperrus M, Tessier E, Berail S, Amouroux D (2016) Investigation of Hg uptake and transport between paddy soil and rice seeds combining Hg isotopic composition and speciation. Elementa: Sci Anthrop 4:00087

    Google Scholar 

  • Gilmour CC, Podar M, Bullock AL, Graham AM, Brown SD, Somenahally AC, Johs A, Hurt RA, Bailey KL, Elias DA (2013) Mercury methylation by novel microorganisms from new environments. Environ Sci Technol 47:11810–11820

    Article  PubMed  CAS  Google Scholar 

  • Hang XS, Gan FQ, Wang JG, Chen XQ, Chen YYD, Wang HY, Zhou JM, Du CW (2016) Soil mercury accumulation and transference to different crop grains. HUM Ecol Risk Assess 22:1242–1252

    Article  CAS  Google Scholar 

  • Heeraman DA, Claassen VP, Zasoski RJ (2001) Interaction of lime, organic matter and fertilizer on growth and uptake of arsenic and mercury by zorro fescue (Vulpia myuros L.). Plant Soil 234:215–231

    Article  CAS  Google Scholar 

  • Horvat M, Nolde N, Fajon V, Jereb V, Logar M, Lojen S, Jacimovic R, Falnoga I, Qu LY, Faganeli J, Damjana D (2003) Total mercury, methylmercury and selenium in mercury polluted areas in the province Guizhou, China. Sci Total Environ 304:231–256

    Article  PubMed  CAS  Google Scholar 

  • Hu HY, Li ZJ, Feng Y, Liu YW, Xue JM, Davis M, Liang YC (2016) Prediction model for mercury transfer from soil to corn grain and its cross-species extrapolation. J Integr Agr 15:2393–2402

    Article  CAS  Google Scholar 

  • Kabata-Pendias A, Pendias H (2001) Trace elements in soil and plants. 3rd edn. CRC Press, Boca Raton.

  • Krupp EM, Mestrot A, Wielgus J, Meharg AA, Feldman J (2009) The molecular form of mercury in biota: identification of novel mercury peptide complexes in plants. Chem Commun 2009:4257–4259

  • Lin Y, Vogt R, Larssen T (2012) Environmental mercury in China: A review. Environ Toxicol Chem 31:2431–2444

    Article  PubMed  CAS  Google Scholar 

  • Li B, Shi JB, Wang X, Meng M, Huang L, Qi XL, He B, Ye ZH (2013) Variations and constancy of mercury and methylmercury accumulation in rice grown at contaminated paddy field sites in three provinces of China. Environ Pollut 181:91–97

    Article  PubMed  CAS  Google Scholar 

  • Li YY, Zhao JT, Zhang BW, Liu YJ, Xu XH, Li YF, Li B, Gao YX, Chai ZF (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 Soil 398:87–97

    Article  CAS  Google Scholar 

  • Li YY, Zhao JT, Guo JX, Liu MJ, Xu QL, Li H, Li YF, Zheng L, Zhang ZY, Gao YX (2017) Influence of sulfur on the accumulation of mercury in rice plant (Oryza sativa L.) growing in mercury contaminated soils. Chemosphere 182:293–300

    Article  PubMed  CAS  Google Scholar 

  • Liang L, Horvat M, Cernichiari E, Gelein 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

    Article  PubMed  CAS  Google Scholar 

  • Liu JL, Feng XB, Qiu GL, Anderson CWN, Yao H (2012) Prediction of methyl mercury uptake by rice plants (Oryza sativa L.) using the diffusive gradient in thin films technique. Environ Sci Technol 46:11013–1101320

    Article  PubMed  CAS  Google Scholar 

  • Mei XQ, Ye ZH, Wong MH (2009) The relationship of root porosity and radial oxygen loss on arsenic tolerance and uptake in rice grains and straw. Environ Pollut 157:2550–2557

    Article  PubMed  CAS  Google Scholar 

  • Meng B, Feng XB, Qiu GL, Cai Y, Wang DY, Li P, Shang LH, Sommar J (2010) Distribution patterns of inorganic mercury and methylmercury in tissues of rice (Oryza sativa L.) plants and possible bioaccumulation pathways. J Agr Food Chem 58:4951–4958

    Article  CAS  Google Scholar 

  • Meng B, Feng XB, Qiu GL, Liang P, Li P, Chen CX, Shang LH (2011) The process of methylmercury accumulation in rice (Oryza sativa L.). Environ Sci Technol 45:2711–2717

    Article  PubMed  CAS  Google Scholar 

  • Meng M, Li B, Shao JJ, Wang T, He B, Shi JB, Ye ZH, Jiang GB (2014a) Accumulation of total mercury and methylmercury in rice plants collected from different mining areas in China. Environ Pollut 184:179–186

    Article  PubMed  CAS  Google Scholar 

  • Meng B, Feng XB, Qiu GL, Anderson CWN, Wang JX, Zhao L (2014b) Localization and speciation of mercury in brown rice with implications for pan-Asian public health. Environ Sci Technol 48:7974–7981

    Article  PubMed  CAS  Google Scholar 

  • Mergler D, Anderson HA, Chan LHM, Mahaffey KR, Murray M, Sakamoto M, Stern AH (2007) Methylmercury exposure and health effects in humans: A world wide concern. Ambio 36:3–11

    Article  PubMed  CAS  Google Scholar 

  • Method 1630 (2001): Methylmercury in Water by Distillation, Aqueous Ethylation, Purge and Trap, and CVAFS, EPA-821-R-01-020; U.S. EPA: Washington, DC.

  • Norton GJ, Duan GL, Dasgupta T, Islam MR, Lei M, Zhu YG, Deacon CM, Moran AC, Islam S, Zhao FJ, Stroud JL, McGrath SP, Feldmann J, Price AH, Meharg AA (2009) Environmental and genetic control of arsenic accumulation and speciation in rice grain: comparing a range of common cultivars grown in contaminated sites across Bangladesh, China, and India. Environ Sci Technol 43:8381–8386

    Article  PubMed  CAS  Google Scholar 

  • Norton GJ, Dasgupta T, Islam MR, Islam S, Deacon CM, Zhao FJ, Stroud JL, McGrath SP, Feldman J, Price AH, Meharg AA (2010) Arsenic influence on genetic variation in grain trace-element nutrient content in Bengal delta grown rice. Environ Sci Technol 44:8284–8288

    Article  PubMed  CAS  Google Scholar 

  • Patty C, Barnett B, Mooney B, Kahn A, Levy S, Liu YJ, Pianetta P, Andrews JC (2009) Using X-ray microscopy and Hg L3 XANES to study Hg binding in the rhizosphere of Spartina cordgrass. Environ Sci Technol 43:7397–7402

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Peng XY, Liu FJ, Wang WX, Ye ZH (2012) Reducing total mercury and methylmercury accumulation in rice grains through water management and deliberate selection of rice cultivars. Environ Pollut 162:202–208

    Article  PubMed  CAS  Google Scholar 

  • Plaza J, Viera M, Donati E, Guibal E (2011) Biosorption of mercury by Macrocystis pyrifera and Undaria pinnatifida: Influence of zinc, cadmium and nickel. J Environ Sci 23:1778–1786

    Article  CAS  Google Scholar 

  • Qian YZ, Chen C, Zhang Q, Li Y, Chen ZJ, Li M (2010) Concentrations of cadmium, lead, mercury and arsenic in Chinese market milled rice and associated population health risk. Food Control 21:1757–1763

    Article  CAS  Google Scholar 

  • Rothenberg SE, Feng XB, Zhou WJ, Tu M, Jin BW, You JM (2012) Environment and genotype controls on mercury accumulation in rice (Oryza sativa L.) cultivated along a contamination gradient in Guizhou, China. Sci Total Environ 426:272–280

    Article  PubMed  CAS  Google Scholar 

  • Rutkowska B, Murawska B, Spychaj-Fabisiak E, Sz R, Szulc W, Piekut A (2016) Evaluation of the mercury content of loamy sand soil after long-term nitrogen and potassium fertilization. Plant Soil Environ 61:537–543

    Article  CAS  Google Scholar 

  • Si YB, Zou Y, Liu XH, Si XY, Mao JD (2015) Mercury methylation coupled to iron reduction by dissimilatory iron-reducing bacteria. Chemosphere 122:206–212

    Article  PubMed  CAS  Google Scholar 

  • Strickman RJ, Mitchell CPJ (2017) Accumulation and translocation of methylmercury and inorganic mercury in Oryza sativa: An enriched isotope tracer study. Sci Total Environ 574:1415–1423

    Article  PubMed  CAS  Google Scholar 

  • Tang WL, Dang F, Evans D, Zhong H, Xiao L (2017) Understanding reduced inorganic mercury accumulation in rice following selenium application: Selenium application routes, speciation and doses. Chemosphere 169:369–376

    Article  PubMed  CAS  Google Scholar 

  • Ullrich SM, Tanton TW, Abdrashitova SA (2001) Mercury in the aquatic environment: A review of factors affecting methylation. Crit Rev Environ Sci Technol 31:241–293

    Article  CAS  Google Scholar 

  • Wang X, Li B, Tam NFY, Huang L, Qi XL, Wang HB, Ye ZH, Meng M, Shi JB (2014a) Radial oxygen loss has different effects on the accumulation of total mercury and methylmercury in rice. Plant Soil 385:343–355

    Article  CAS  Google Scholar 

  • Wang X, Ye ZH, Li B, Huang L, Meng M, Shi JB, Jiang GB (2014b) Growing rice aerobically markedly decreases mercury accumulation by reducing both Hg bioavailability and the production of MeHg. Environ Sci Technol 48:1878–1885

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Tam NFY, Fu S, Ametkhan A, Ouyang Y, Ye ZH (2014c) Selenium addition alters mercury uptake, bioavailability in the rhizosphere and root anatomy of rice (Oryza sativa). Ann Bot 114:271–278

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang X, Tam NFY, He HD, Ye ZH (2015) The role of root anatomy, organic acids and iron plaque on mercury accumulation in rice. Plant Soil 394:301–313

    Article  CAS  Google Scholar 

  • Wang YJ, Dang F, Zhao JT, Zhong H (2016a) Selenium inhibits sulfate-mediated methylmercury production in rice paddy soil. Environ Pollut 213:232–239

    Article  PubMed  CAS  Google Scholar 

  • Wang YJ, Dang F, Evans RD, Zhong H, Zhao JT, Zhou DM (2016b) Mechanistic understanding of MeHg-Se antagonism in soil-rice systems: The key role of antagonism in soil. Sci Rep 6:19477

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Warner KA, Roden EE, Bonzongo JC (2003) Microbial mercury transformation in anoxic freshwater sediments under iron-reducing and other electron-accepting conditions. Environ Sci Technol 37:2159–2165

    Article  PubMed  CAS  Google Scholar 

  • Yin R, Feng XB, Meng B (2013) Stable mercury isotope variation in rice plants (Oryza sativa L.) from the Wanshan mercury mining district, SW China. Environ Sci Technol 47:2238–2245

    Article  PubMed  CAS  Google Scholar 

  • Yu RQ, Flanders JR, Mack EE, Turner R, Mirza MB, Barkay T (2011) Contribution of coexisting sulfate and iron reducing bacteria to methylmercury production in freshwater river sediments. Sci Total Environ 46(5):2684–2691

    Article  CAS  Google Scholar 

  • Zhang L, Wong MH (2007) Environmental mercury contamination in China: Sources and impacts. Environ Int 33:108–121

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Feng XB, Larssen T, Shang LH, Li P (2010) Bioaccumulation of methylmercury versus inorganic mercury in rice (Oryza sativa L.) grain. Environ Sci Technol 44:4499–4504

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Feng XB, Zhu JM, Sapkota A, Meng B, Yao H, Qin HB, Larssen T (2012) Selenium in soil inhibits mercury uptake and translocation in rice (Oryza sativa L.). Environ Sci Technol 46:10040–10046

    PubMed  CAS  Google Scholar 

  • Zhao L, Qiu GL, Anderson CWN, Meng B, Wang DY, Shang LH, Yan HY, Feng XB (2016) Mercury methylation in rice paddies and its possible controlling factors in the Hg mining area, Guizhou province, Southwest China. Environ Pollut 215:1–9

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The work described in this article was supported by the National Key Research and Development Program of China (2016YFD0800306), NSFC-Guangdong United Foundation (U1501232), and the National Natural Science Foundation of China (31670409, 31070450). The authors would like to thank Dean Meyer, PhD, ELS, from Liwen Bianji, Edanz Group China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript. We also thank Prof. A.J.M. Baker (The Universities of Melbourne and Queensland, Australia) for help in the further improvement of this paper.

Author information

Author notes

  1. Lu Huang and Bing Li contributed equally to this work.

Authors and Affiliations

  1. School of Life Sciences, Sun Yat-sen University, University Town, Guangzhou, 510006, People’s Republic of China

    Lu Huang & Zhihong Ye

  2. Guiyang Research Academy of Eco-Environmental Sciences, Guiyang 550002, China

    Bing Li

  3. Department of Chemistry, City University of Hong Kong, Kowloon, Hong Kong, SAR,, China

    Nora Fung-Yee Tam

  4. College of Marine Sciences, South China Agricultural University, Guangzhou 510642, China

    Xun Wang

Authors
  1. Lu Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bing Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nora Fung-Yee Tam
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhihong Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhihong Ye.

Additional information

Responsible Editor: Juan Barcelo.

Electronic supplementary material

ESM 1

(DOCX 19 kb)

ESM 2

(DOCX 18.3 kb)

ESM 3

(DOCX 106 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, L., Li, B., Tam, N.FY. et al. Effects of environment and genotype on mercury and methylmercury accumulation in rice (Oryza sativa L.). Plant Soil 427, 269–280 (2018). https://doi.org/10.1007/s11104-018-3651-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-018-3651-4

Keywords

Search

Navigation