Elsevier

Science of The Total Environment

Volume 475, 15 March 2014, Pages 83-89
Science of The Total Environment

Antimony uptake, translocation and speciation in rice plants exposed to antimonite and antimonate

https://doi.org/10.1016/j.scitotenv.2013.12.103Get rights and content

Highlights

  • We examined the impact of iron plaque on different species of Sb uptake by rice.

  • Iron plaque accumulated more Sb than rice plants and affected SbIII and SbV uptake by rice roots.

  • Rice was much more efficient in taking up SbIII than SbV, and SbV was the predominant Sb species in rice plants.

  • Sb was mostly localized to the cell walls of rice plants, resulting in limited translocation from the roots to shoots.

Abstract

Antimony (Sb) accumulation in rice is a potential threat to human health, but its uptake mechanisms are unclear. A hydroponic experiment was conducted to investigate uptake, translocation, speciation and subcellular distribution of Sb in rice plants exposed to antimonite (SbIII) and antimonate (SbV) at 0.2, 1.0 or 5.0 mg/L for 4 h. More Sb was accumulated in iron plaque than in the plant, with both the roots (~ 10–12 times) and Fe plaque (~ 28–54 times) sequestering more SbIII than SbV. The presence of iron plaque decreased uptake of both SbV and SbIII. SbIII uptake kinetics fitted better to the Michaelis–Menten function than SbV. Antimonate (56 to 98%) was the predominant form in rice plant with little methylated species being detected using HPLC–ICP-MS. Cell walls accumulated more Sb than organelles and cytosol, which were considered as the first barrier against Sb entering into cells. Sb transformation and subcellular distribution can help to understand the metabolic mechanisms of Sb in rice.

Introduction

Antimony (Sb) is considered a priority environmental pollutant by the United States Environmental Protection Agency and the European Union. It has no known biological function and can be toxic at elevated concentrations. Antimonite (SbIII) and antimonate (SbV) are the common species of Sb in the environment and they can be taken up by plants from soil, causing adverse health effects to human. As a metalloid, its environmental behavior has received little attention though it is gaining interest as a global contaminant (Wilson et al., 2010).

The maximum allowable Sb level in drinking water is 5 μg/L in China whereas the World Health Organization (WHO) sets safe drinking water level for Sb at 20 μg/L (He et al., 2012). Anthropogenic activities such as mining, smelting, fossil fuel combustion and waste incineration have elevated Sb levels in the environment. Landrum et al. (2009) recently reported values of 1.12–4.19 mg/L Sb in water from El Tatio Geyser field in Chile. The Sb concentrations in the seepage water from leakage of a smelter in Hunan, China are elevated, ranging from 8.4 to 11 mg/L (He, 2007). The Sb concentration in paddy soils near Xikuangshan Sb mine area in Hunan, China reached 1565 mg/kg (He and Yang, 1999), which was much greater than 36 mg/kg, the maximum permissible pollutant concentrations for Sb recommended by WHO in soils (Chang et al., 2002). Rice plants accumulate high concentration of Sb up to 225 mg/kg in the roots and 5.79 mg/kg in the seeds. Hence, it is important to study Sb behavior in the environment.

Rice is a major food crop for 3 billion people, especially in Asian countries. Rice has been implicated as a major route for Sb exposure, especially in mining areas. The Sb concentrations in rice near the Xikuangshan Sb mine were 160–930 μg/kg (Wu et al., 2011b). According to WHO, rice contributes 33% of the total daily intake of Sb, which is higher than other exposure routes. However, limited data are available regarding Sb uptake and translocation in rice plants. Sb negatively impacts rice growth, with rice yield dropping by 10% when SbIII and SbV concentrations are 150 and 300 mg/kg in soils (He and Yang, 1999). Feng et al. (2011a) found that more Sb is concentrated in rice shoots than roots after 14 d exposure to 5 mg/L SbIII under hydroponic conditions. However, SbIII can be oxidized to SbV rapidly in solution. So it is necessary to study SbIII and SbV uptake by rice in short term to minimize SbIII transformation in solution.

Mechanisms of arsenic uptake have been studied extensively in rice plants (Meharg and Jardine, 2003, Zhao et al., 2010). Arsenite (AsIII) and arsenate (AsV) are taken up by aquaporin channels and phosphate transporters by rice, with AsV being reduced to AsIII in root cells. By contrast, little is known about the mechanism of uptake, speciation, and transformation of Sb in rice plants. Okkenhaug et al. (2012) found that SbV is the main species in rice roots and shoots, with > 90% of Sb being SbV in porewater in pots. He and Yang (1999) investigated SbIII and SbV accumulation in rice without considering Sb speciation. Huang et al. (2011) studied the influence of Fe plaque on Sb uptake and translocation in rice without considering Sb speciation. It is known that SbIII is more toxic than SbV, so it is necessary to understand Sb transformation in rice to better assess its toxicity.

In addition, subcellular distribution of toxic elements can help to understand their translocation and detoxification mechanism in plants. Cr is mainly associated with cell walls in rice plants (Zeng et al., 2011) so is most of Cd (He et al., 2008). However, information about the subcellular distribution of Sb in rice has rarely been documented.

As a waterlogged plant, rice grows in anaerobic environment and releases oxygen to its rhizosphere through developed aerenchyma (Winkel et al., 2013). The oxygen oxidizes ferrous iron (FeII) to form iron plaque coating on the root surfaces (Zhao et al., 2010). Iron plaque has been shown to have a high affinity for AsV, playing an important role in As uptake by rice. Fe plaque may be responsible for AsIII oxidation to AsV, reducing As toxicity (Zhao et al., 2009). Sb and As are chemical analogs so we hypothesized that Sb uptake and speciation in rice was similar to As. Huang et al. (2011) reported that Sb accumulation by rice is influenced by Fe plaque on root surface, with 40–80% of total Sb being accumulated in Fe plaque. However, the direct role of iron plaque in Sb uptake into rice roots needs further investigation.

The overall goal of this study was to examine the uptake, translocation and speciation of Sb by rice plants exposed to SbIII and SbV. Our specific objectives were to: 1) evaluate the effects of iron plaque on Sb accumulation in rice plants; 2) investigate Sb distribution and speciation in rice plants; and 3) study Sb subcellular distribution in rice plants.

Section snippets

Germination and cultivation of rice plants

Rice seeds (Oryza sativa L., Nanjing 45) were surface sterilized by soaking them in 30% H2O2 solution for 15 min and then rinsed in Milli-Q water. They were then soaked in Milli-Q water for 48 h, and germinated on moistened filter papers placed in a petri dish. After germination, they were transferred to a 96-orifice plate. At one-leaf stage, they were treated with 0.25-strength nutrition solution recommended by International Rice Research Institute (Wu et al., 2011a). At three-leaf stage, they

Results and discussion

Antimony speciation in the growth media was determined after exposing rice plants to 0.2, 1 and 5 mg/L SbIII or SbV for 4 h (Table 1). After 4 h exposure, 6.20–38.1% of the SbIII was oxidized to SbV while SbV was stable. This indicated that SbIII was unstable during the 4 h experiment and both SbIII and SbV existed in the SbIII treatment.

Conclusion

In conclusion, SbIII oxidization to SbV in solution was observed after exposing rice plants for 4 h. More Sb was accumulated on Fe plaque than rice roots, which affected Sb accumulation in rice. SbIII and SbV uptake kinetics by excised rice roots were described by Michaelis–Menten function. Rice was more efficient in SbIII than SbV uptake with most of the Sb being accumulated in the roots as being SbV. Plant cell walls may have acted as key storage compartment for Sb in rice.

Acknowledgments

This work was supported in part by the National Natural Science Foundation of China (No. 21277070) and Jiangsu Provincial Innovation Fund.

References (35)

  • M. Vithanage et al.

    Surface complexation modeling and spectroscopic evidence of antimony adsorption on iron-oxide-rich red earth soils

    J Colloid Interface Sci

    (2013)
  • S.C. Wilson et al.

    The chemistry and behaviour of antimony in the soil environment with comparisons to arsenic: a critical review

    Environ Pollut

    (2010)
  • F. Wu et al.

    Health risk associated with dietary co-exposure to high levels of antimony and arsenic in the world's largest antimony mine area

    Sci Total Environ

    (2011)
  • R. Zangi et al.

    Transport routes of metalloids into and out of the cell: a review of the current knowledge

    Chem Biol Interact

    (2012)
  • P.F. Bell et al.

    Plant uptake of 14C-EDTA, 14C-Citrate, and 14C-Histidine from chelator-buffered and conventional hydroponic solutions

    Plant Soil

    (2003)
  • A. Chang et al.

    Developing human health-related chemical guidelines for reclaimed water and sewage sludge applications in agriculture

    (2002)
  • M. He

    Distribution and phytoavailability of antimony at an antimony mining and smelting area, Hunan, China

    Environ Geochem Health

    (2007)
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