Environ Sci Pollut Res DOI 10.1007/s11356-014-4065-3
REVIEW ARTICLE
Recent advances in arsenic bioavailability, transport, and speciation in rice Xin Wang & Bo Peng & Changyin Tan & Lena Ma & Bala Rathinasabapathi
Received: 22 September 2014 / Accepted: 30 December 2014 # Springer-Verlag Berlin Heidelberg 2015
Abstract Widespread arsenic (As) contamination in paddy rice (Oryza sativa) from both geologic and anthropogenic origins is an increasing concern globally. Substantial efforts have been made to elucidate As transformation and uptake processes in rhizosphere and metabolism in rice plant, which provides an essential foundation for the development of mitigation strategies. However, a range of crucial mechanisms from As mobilization in rhizosphere to transport to grains remain poorly understood. To provide new insight into the underlying mechanisms of As accumulation in rice, a range of new perspectives on As bioavailability, transport pathways, and in situ speciation are reviewed here. Specifically, the prominent effects of water regime, Fe plaque, and biochar on As mobilization in rice rhizosphere are discussed critically. An updated understanding of arsenite (AsIII) and methylated As transport from root to vascular bundle and grain is integrated and discussed in detail. Special attention is given to As speciation and distribution in rice grain with potential coping strategies being provided and discussed. Future research priorities are also identified. The new insight into As Responsible editor: Philippe Garrigues X. Wang (*) : B. Peng : C. Tan College of Resources and Environmental Science, Hunan Normal University, Changsha 410081, Hunan, China e-mail: [email protected] L. Ma Soil and Water Science Department, University of Florida, Gainesville, FL 32611, USA L. Ma State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, Jiangsu 210046, China B. Rathinasabapathi Horticultural Sciences Department, University of Florida, Gainesville, FL 32611, USA
bioavailability, transport and speciation in rice would lead to a better understanding of As contamination in rice. They would also provide useful strategies from agronomic measures to genetic engineering for more effective restriction of As transport and accumulation in food chain. Keywords Arsenite . Biochar . Transport . Speciation . Rice grain
Introduction Rice, the staple food feeding half the world’s population, is the most efficient in arsenic (As) uptake and accumulation among cereal crops. As a result, widespread As contamination in rice grain has occurred through the soil-water-rice pathway. In South and Southeast Asia, the geochemical occurrence of As in groundwater has been regarded as the worst environmental disaster in human history (Meharg 2004). In Bangladesh, the area with the most severe As poisoning in shallow underground aquifers, more than 1000 t of As has been imported into the cultivated land through irrigation with As-enriched groundwater (Zhao et al. 2010a), posing serious risks to human health and sustainable agriculture. In parallel, another tragedy caused by anthropogenic As contamination has been taking place in Hunan province, which is considered as the heartland of Chinese nonferrous mining and smelting. As a result of the long-term discharge of As-containing drainage, improper storage of tailings, and deposition of metallurgical fume, elevated As in rice grains up to 723 ng g−1 has been determined in mine-affected districts across the province, far exceeding the Chinese maximum contaminant level of 150 ng g−1 for inorganic As in rice (Zhu et al. 2008; Williams et al. 2009a; Okkenhaug et al. 2012). In particular, As mining and processing activities in Shimen realgar mine (Changde, Hunan), which had the largest realgar deposit in Asia, has
Environ Sci Pollut Res
resulted in the worst As poisoning in local food chains with surface water containing up to 64.6 mg L−1 As. Emerging evidence has confirmed that rice is an important dietary source of As exposure and may lead to adverse health outcomes, particularly in South and Southeast Asia where rice is consumed as the primary source of caloric intake. For example, a recent study of 18,470 Bangladeshis has revealed a significant association of rice consumption with both urinary As and prevalent skin lesions (Melkonian et al. 2013). Similarly, another study targeting pregnant women in USA has shown a remarkably positive correlation between rice intake and urinary As, with the latter being regarded as a reliable biomarker of individual As exposure (Gilbert-Diamond et al. 2011). To mitigate As accumulation in rice, numerous studies have been carried out towards better understanding of As rhizosphere processes, root uptake, vascular transport, and grain unloading of As (Ma et al. 2008; Meharg et al. 2008; Xu et al. 2008; Lombi et al. 2009; Zhao et al. 2009, Zhao et al. 2010a, b; Seyfferth et al. 2010; Carey et al. 2010; Zhao et al. 2013a). To update our understanding of As contamination in rice, the recent progress in As bioavailability, in vivo transport, and speciation in this staple food is overviewed critically here. Particularly, (1) some newly reported effect of Fe plaque, radial oxygen loss, and biochar on As mobilization in rice rhizosphere is discussed in detail; (2) the effect of Si amendment on AsIII transport and the probable role of plasma membrane intrinsic proteins (PIP) in AsIII uptake is evaluated critically. Moreover, in situ high resolution of As speciation and distribution in rice root is fully analyzed; (3) an updated understanding of methylated As transport in grain filling is also synthesized. Throughout this review, the environmental significance of these progresses and potential strategies are highlighted with research priorities being also identified.
Arsenic bioavailability in rice rhizosphere Paddy rice is particularly affected by As contamination in soils as it is generally grown under flooded conditions where arsenate (AsV) is largely reduced to AsIII and readily desorbed from soil solid phase, leading to elevated AsIII bioavailability (Stroud et al. 2011). For example, in a greenhouse-scale experiment with 14 paddy soils from Bangladesh, China, and UK, up to 13 mg L−1 As was determined in soil pore water with AsIII accounting for >95 % of total soluble As under flooded condition (Khan et al. 2010). Moreover, such As mobilization into aqueous phase is greatly promoted by reductive dissolution of iron (Fe) oxyhydroxides under anoxic conditions. For instance, in a field-scale experiment, As in intermittently flooded conditions was decreased by 86 % in pore water, 55 % in the root plaque, and 41 % in rice grains compared to the continuously flooded plots (Somenahally et al. 2011).
Simultaneously, relatively higher abundance of Fe-reducing bacteria was determined under continuous flooding conditions than the intermittent flood treatment (Somenahally et al. 2011), highlighting the risks of elevated As mobility from reductive dissolution of Fe oxides followed by the release and reduction of associated As. Based on these studies, it is conceivable that water management plays a crucial role in As accumulation in rice by directly controlling As solubility and bioavailability. As bioavailability in paddy soil is also closely associated with soil mineralogy. In most cases, Fe oxides/hydroxides represent the major pool of As in soils (Dixit and Hering 2003; Miretzky and Cirelli 2010). Therefore, As solubility is strongly controlled by As adsorption on Fe (hydr)oxides in paddy soils. In a recent study, rapid coprecipitation of exogenous AsV with dissolved FeIII/FeII from aqueous phase was determined in anoxic soils (Fan et al. 2014), which could favor As immobilization by preventing AsV reduction to AsIII. On the other hand, in rice rhizosphere, as a result of oxygen release via rice aerenchyma, Fe plaque commonly forms on root surfaces and mainly comprises amorphous or crystalline Fe (oxyhydr)oxides (e.g., γ-FeOOH, α-FeOOH, Fe(OH)3nH2O), which can retard As flow towards roots by sorbing it (Liu et al. 2006; Wu et al. 2011; Syu et al. 2013). For example, elevated ratio of As to Fe has been determined in Fe plaque around rice roots relative to Fe minerals in soil matrix, indicating a high capacity of Fe plaque for As retention in rhizosphere (Yamaguchi et al. 2014). However, it should be noted that the predominance of AsIII in Fe plaque under anaerobic condition may enhance AsIII influx into rice (Yamaguchi et al. 2014) considering the lower affinity of Fe plaque to AsIII than to AsV (Liu et al. 2005). Besides, under flooded condition, young rice roots and the younger portion of mature roots had little or no Fe plaque based on X-ray fluorescence images (Seyfferth et al. 2010, 2011; Yamaguchi et al. 2014). This could be due to the lack of aerenchyma of younger portion of root close to root apex and decreased soil redox potential (Eh) at deeper layer (Butterbach-Bahl et al. 2000; Yamaguchi et al. 2014). In the absence of Fe plaque, both AsV and AsIII could move efficiently into rice through the fine and young roots which are generally considered as the most important portion for nutrient and pollutant uptake (Marschner 2003). Drainage of floodwater before harvest can induce the shift from anaerobic to aerobic condition, which occurs first around rice root with AsV becoming the dominant species in Fe plaque (Yamaguchi et al., 2014). Given that oxidative reaction takes place faster than the shift to highly reductive condition (Nakamura and Katou 2012), intermittent drainage particularly during grain filling could be effective for immobilizing AsV in Fe plaque and thus limits As influx into rice. In addition, the rate of oxygen diffusion into rhizosphere through root aerenchyma, which is termed radial oxygen loss (ROL), has also been identified to exert a significant effect on As
Environ Sci Pollut Res
bioavailability (Mei et al. 2012; Pan et al. 2014). The rate of ROL varies widely among different genotypes (Mei et al. 2009; Lee et al. 2013; Wu et al. 2013a). The genotypes with higher ROL rate tend to have higher Fe and As accumulation in Fe plaque, leading to decreased As mobilization in rice rhizosphere and hence diminished shoot and grain As translocation (Mei et al. 2012; Pan et al. 2014). Therefore, screening or breeding rice cultivars with high rate of ROL could be developed as useful measure to decrease As bioavailability in rice rhizosphere. In paddy fields, dissolved organic carbon (DOC) tends to enhance As mobilization. There was a significant positive correlation between pore water As and DOC (p
REVIEW ARTICLE
Recent advances in arsenic bioavailability, transport, and speciation in rice Xin Wang & Bo Peng & Changyin Tan & Lena Ma & Bala Rathinasabapathi
Received: 22 September 2014 / Accepted: 30 December 2014 # Springer-Verlag Berlin Heidelberg 2015
Abstract Widespread arsenic (As) contamination in paddy rice (Oryza sativa) from both geologic and anthropogenic origins is an increasing concern globally. Substantial efforts have been made to elucidate As transformation and uptake processes in rhizosphere and metabolism in rice plant, which provides an essential foundation for the development of mitigation strategies. However, a range of crucial mechanisms from As mobilization in rhizosphere to transport to grains remain poorly understood. To provide new insight into the underlying mechanisms of As accumulation in rice, a range of new perspectives on As bioavailability, transport pathways, and in situ speciation are reviewed here. Specifically, the prominent effects of water regime, Fe plaque, and biochar on As mobilization in rice rhizosphere are discussed critically. An updated understanding of arsenite (AsIII) and methylated As transport from root to vascular bundle and grain is integrated and discussed in detail. Special attention is given to As speciation and distribution in rice grain with potential coping strategies being provided and discussed. Future research priorities are also identified. The new insight into As Responsible editor: Philippe Garrigues X. Wang (*) : B. Peng : C. Tan College of Resources and Environmental Science, Hunan Normal University, Changsha 410081, Hunan, China e-mail: [email protected] L. Ma Soil and Water Science Department, University of Florida, Gainesville, FL 32611, USA L. Ma State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, Jiangsu 210046, China B. Rathinasabapathi Horticultural Sciences Department, University of Florida, Gainesville, FL 32611, USA
bioavailability, transport and speciation in rice would lead to a better understanding of As contamination in rice. They would also provide useful strategies from agronomic measures to genetic engineering for more effective restriction of As transport and accumulation in food chain. Keywords Arsenite . Biochar . Transport . Speciation . Rice grain
Introduction Rice, the staple food feeding half the world’s population, is the most efficient in arsenic (As) uptake and accumulation among cereal crops. As a result, widespread As contamination in rice grain has occurred through the soil-water-rice pathway. In South and Southeast Asia, the geochemical occurrence of As in groundwater has been regarded as the worst environmental disaster in human history (Meharg 2004). In Bangladesh, the area with the most severe As poisoning in shallow underground aquifers, more than 1000 t of As has been imported into the cultivated land through irrigation with As-enriched groundwater (Zhao et al. 2010a), posing serious risks to human health and sustainable agriculture. In parallel, another tragedy caused by anthropogenic As contamination has been taking place in Hunan province, which is considered as the heartland of Chinese nonferrous mining and smelting. As a result of the long-term discharge of As-containing drainage, improper storage of tailings, and deposition of metallurgical fume, elevated As in rice grains up to 723 ng g−1 has been determined in mine-affected districts across the province, far exceeding the Chinese maximum contaminant level of 150 ng g−1 for inorganic As in rice (Zhu et al. 2008; Williams et al. 2009a; Okkenhaug et al. 2012). In particular, As mining and processing activities in Shimen realgar mine (Changde, Hunan), which had the largest realgar deposit in Asia, has
Environ Sci Pollut Res
resulted in the worst As poisoning in local food chains with surface water containing up to 64.6 mg L−1 As. Emerging evidence has confirmed that rice is an important dietary source of As exposure and may lead to adverse health outcomes, particularly in South and Southeast Asia where rice is consumed as the primary source of caloric intake. For example, a recent study of 18,470 Bangladeshis has revealed a significant association of rice consumption with both urinary As and prevalent skin lesions (Melkonian et al. 2013). Similarly, another study targeting pregnant women in USA has shown a remarkably positive correlation between rice intake and urinary As, with the latter being regarded as a reliable biomarker of individual As exposure (Gilbert-Diamond et al. 2011). To mitigate As accumulation in rice, numerous studies have been carried out towards better understanding of As rhizosphere processes, root uptake, vascular transport, and grain unloading of As (Ma et al. 2008; Meharg et al. 2008; Xu et al. 2008; Lombi et al. 2009; Zhao et al. 2009, Zhao et al. 2010a, b; Seyfferth et al. 2010; Carey et al. 2010; Zhao et al. 2013a). To update our understanding of As contamination in rice, the recent progress in As bioavailability, in vivo transport, and speciation in this staple food is overviewed critically here. Particularly, (1) some newly reported effect of Fe plaque, radial oxygen loss, and biochar on As mobilization in rice rhizosphere is discussed in detail; (2) the effect of Si amendment on AsIII transport and the probable role of plasma membrane intrinsic proteins (PIP) in AsIII uptake is evaluated critically. Moreover, in situ high resolution of As speciation and distribution in rice root is fully analyzed; (3) an updated understanding of methylated As transport in grain filling is also synthesized. Throughout this review, the environmental significance of these progresses and potential strategies are highlighted with research priorities being also identified.
Arsenic bioavailability in rice rhizosphere Paddy rice is particularly affected by As contamination in soils as it is generally grown under flooded conditions where arsenate (AsV) is largely reduced to AsIII and readily desorbed from soil solid phase, leading to elevated AsIII bioavailability (Stroud et al. 2011). For example, in a greenhouse-scale experiment with 14 paddy soils from Bangladesh, China, and UK, up to 13 mg L−1 As was determined in soil pore water with AsIII accounting for >95 % of total soluble As under flooded condition (Khan et al. 2010). Moreover, such As mobilization into aqueous phase is greatly promoted by reductive dissolution of iron (Fe) oxyhydroxides under anoxic conditions. For instance, in a field-scale experiment, As in intermittently flooded conditions was decreased by 86 % in pore water, 55 % in the root plaque, and 41 % in rice grains compared to the continuously flooded plots (Somenahally et al. 2011).
Simultaneously, relatively higher abundance of Fe-reducing bacteria was determined under continuous flooding conditions than the intermittent flood treatment (Somenahally et al. 2011), highlighting the risks of elevated As mobility from reductive dissolution of Fe oxides followed by the release and reduction of associated As. Based on these studies, it is conceivable that water management plays a crucial role in As accumulation in rice by directly controlling As solubility and bioavailability. As bioavailability in paddy soil is also closely associated with soil mineralogy. In most cases, Fe oxides/hydroxides represent the major pool of As in soils (Dixit and Hering 2003; Miretzky and Cirelli 2010). Therefore, As solubility is strongly controlled by As adsorption on Fe (hydr)oxides in paddy soils. In a recent study, rapid coprecipitation of exogenous AsV with dissolved FeIII/FeII from aqueous phase was determined in anoxic soils (Fan et al. 2014), which could favor As immobilization by preventing AsV reduction to AsIII. On the other hand, in rice rhizosphere, as a result of oxygen release via rice aerenchyma, Fe plaque commonly forms on root surfaces and mainly comprises amorphous or crystalline Fe (oxyhydr)oxides (e.g., γ-FeOOH, α-FeOOH, Fe(OH)3nH2O), which can retard As flow towards roots by sorbing it (Liu et al. 2006; Wu et al. 2011; Syu et al. 2013). For example, elevated ratio of As to Fe has been determined in Fe plaque around rice roots relative to Fe minerals in soil matrix, indicating a high capacity of Fe plaque for As retention in rhizosphere (Yamaguchi et al. 2014). However, it should be noted that the predominance of AsIII in Fe plaque under anaerobic condition may enhance AsIII influx into rice (Yamaguchi et al. 2014) considering the lower affinity of Fe plaque to AsIII than to AsV (Liu et al. 2005). Besides, under flooded condition, young rice roots and the younger portion of mature roots had little or no Fe plaque based on X-ray fluorescence images (Seyfferth et al. 2010, 2011; Yamaguchi et al. 2014). This could be due to the lack of aerenchyma of younger portion of root close to root apex and decreased soil redox potential (Eh) at deeper layer (Butterbach-Bahl et al. 2000; Yamaguchi et al. 2014). In the absence of Fe plaque, both AsV and AsIII could move efficiently into rice through the fine and young roots which are generally considered as the most important portion for nutrient and pollutant uptake (Marschner 2003). Drainage of floodwater before harvest can induce the shift from anaerobic to aerobic condition, which occurs first around rice root with AsV becoming the dominant species in Fe plaque (Yamaguchi et al., 2014). Given that oxidative reaction takes place faster than the shift to highly reductive condition (Nakamura and Katou 2012), intermittent drainage particularly during grain filling could be effective for immobilizing AsV in Fe plaque and thus limits As influx into rice. In addition, the rate of oxygen diffusion into rhizosphere through root aerenchyma, which is termed radial oxygen loss (ROL), has also been identified to exert a significant effect on As
Environ Sci Pollut Res
bioavailability (Mei et al. 2012; Pan et al. 2014). The rate of ROL varies widely among different genotypes (Mei et al. 2009; Lee et al. 2013; Wu et al. 2013a). The genotypes with higher ROL rate tend to have higher Fe and As accumulation in Fe plaque, leading to decreased As mobilization in rice rhizosphere and hence diminished shoot and grain As translocation (Mei et al. 2012; Pan et al. 2014). Therefore, screening or breeding rice cultivars with high rate of ROL could be developed as useful measure to decrease As bioavailability in rice rhizosphere. In paddy fields, dissolved organic carbon (DOC) tends to enhance As mobilization. There was a significant positive correlation between pore water As and DOC (p
