Mitigation of Arsenic Accumulation in Rice with Water Management

Apr 14, 2009 - Soil Science Department, Rothamsted Research, Harpenden,. Hertfordshire ... and Research Institute for Bioresources, Okayama University...
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Environ. Sci. Technol. 2009, 43, 3778–3783

Mitigation of Arsenic Accumulation in Rice with Water Management and Silicon Fertilization R . Y . L I , †,‡ J . L . S T R O U D , † J . F . M A , § S . P . M C G R A T H , † A N D F . J . Z H A O * ,† Soil Science Department, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, U.K., Nanjing University of Information Science and Technology, Nanjing 210044, China, and Research Institute for Bioresources, Okayama University, Chuo 2-20-1, Kurashiki 710-0046, Japan

Received December 22, 2008. Revised manuscript received February 19, 2009. Accepted March 14, 2009.

Rice represents a major route of As exposure in populations that depend on a rice diet. Practical measures are needed to mitigate the problem of excessive As accumulation in paddy rice. Two potential mitigation methods, management of the water regime and Si fertilization, were investigated under greenhouse conditions. Growing rice aerobically during the entire rice growth duration resulted in the least As accumulation. Maintaining aerobic conditions during either vegetative or reproductive stage of rice growth also decreased As accumulation in rice straw and grain significantly compared with rice grown under flooded conditions. The effect of water management regimes was consistent with the observed effect of floodinginduced arsenite mobilization in the soil solution. Aerobic treatments increased the percentage of inorganic As in grain, but the concentrations of inorganic As remained lower than in the flooded rice. Silicon fertilization decreased the total As concentration in straw and grain by 78 and 16%, respectively, even though Si addition increased As concentration in the soil solution. Silicon also significantly influenced As speciation in rice grain and husk by enhancing methylation. Silicon decreased the inorganic As concentration in grain by 59% while increasing the concentration of dimethylarsinic acid (DMA) by 33%. There were also significant differences between two rice genotypes in grain As speciation. This study demonstrated that water management, Si fertilization, and selection of rice cultivars are effective measures that can be used to reduce As accumulation in rice.

1. Introduction Arsenic is a nonthreshold carcinogen. Recent studies have shown that consumption of rice constitutes a large proportion of dietary intake of inorganic As in populations in south and southeast Asia not exposed to As-contaminated drinking water (1, 2). Even in As-affected areas in Bangladesh and West Bengal, India, rice is a major exposure route of As, representing about half of the total As intake (3, 4). A global survey of ∼900 samples of polished market rice shows a range of total As from 0.01 to 0.82 mg kg-1, with a mean and median * Corresponding author phone: 44 1582 763133; fax: 44 1582 469036; e-mail: [email protected]. † Rothamsted Research. ‡ Nanjing University of Information Science and Technology. § Okayama University. 3778

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of 0.15 and 0.13 mg kg-1, respectively (2). The estimated potential cancer risk associated with the intake of inorganic As from rice is significant for populations relying on rice in their diet (2, 4). Rice As concentration may be further elevated in areas impacted by mining activities, irrigation of Ascontaminated groundwaters, and past uses of arsenical pesticides. In Bangladesh, As-contaminated water extracted from shallow tube-wells is widely used to irrigate rice crops during the dry season (5), which has resulted in elevated As concentrations in rice grain, up to 1.7 mg kg-1 in some cases (6), and significant yield losses due to As phytotoxicity (7). Rice straw, containing much higher levels of As than grain, is widely used as cattle feed, thus presenting another route of As entry into the food chain (7-9). Paddy rice is more efficient in As uptake than other cereal crops (10), and the underlying reasons have been identified recently. First, anaerobic conditions in paddy soil leads to arsenite mobilization and thus enhanced bioavailability to rice plants (11, 12). Rice grown under flooded conditions was found to accumulate much more As than that grown under aerobic conditions (12). Second, arsenite shares the highly efficient silicon (Si) uptake pathway in rice (13). Two Si transporter proteins, Lsi1 and Lsi2, respectively, mediate the entry of silicic acid into root cells and the efflux from cells to apoplast in the direction of stele for the translocation to the shoots (14, 15). Both transporters, which are highly expressed in rice roots, can also transport arsenite (13). Lsi2 plays a particularly important role in the root to shoot transport of arsenite and As accumulation in rice grain. Among the As nonhyperaccumulators tested, rice has the highest As mobility in the xylem transport (16). A recent greenhouse study showed a strong negative relationship between Si concentration in soil solution and rice As concentration in six paddy soils (17), which is consistent with an antagonistic effect of Si on As accumulation. Chemical speciation of As influences its toxicity to humans. Inorganic As is generally considered to be more toxic than methylated As compounds (18, 19). While inorganic As is the predominant species of As in rice straw (8), methylated species (mainly dimethylarsinic acid, DMA) can account for from very little to 80% of the total As in rice grain (2, 20-22). The pathway of As methylation in microorganisms is well-established, but in higher plants the genes responsible for As methylation have not been identified (16). The relationship between inorganic As and total grain As has been investigated recently (2, 21). It appears that rice produced in the United States, while generally containing higher levels of total As, has a lower slope of inorganic As versus total As than rice produced in Asian countries, indicating a greater proportion of DMA in US rice (2, 21). The reasons for the large variation in the inorganic As and DMA proportions are largely unknown, although both genetic and environmental factors are implicated (2, 21). There is an urgent need to develop mitigation measures to reduce As accumulation in rice. Xu et al. (12) showed that maintaining aerobic conditions throughout the entire growth duration was a highly effective way of decreasing As accumulation by rice. In the present study, we extended the investigation on the effect of water management by including periodic aerobic treatments, which are likely to be more practical for rice cultivation than continuous aerobic conditions. Furthermore, based on the recent evidence that arsenite is taken up by rice through the Si transport pathway (13), we investigated the effectiveness of Si fertilization on mitigating excessive As accumulation by rice. In both experiments, plant As uptake was related to the As dynamics in the soil solution 10.1021/es803643v CCC: $40.75

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phase. In addition, we evaluated the effect of the water management regime and Si fertilization on As speciation in rice grain.

2. Materials and Methods Pot Experiments. Two pot experiments were conducted using a silty clay loam (Aquic Paleudalf, USDA classification) collected from the plow layer (0-20 cm) of an arable field on the Rothamsted farm, Southeast England. The soil contained 1.42% organic C, 0.13% total N, and 11.6 mg kg-1 total As and had a pH of 5.2. The soil total As is slightly elevated compared with background values of grain. Different water management regimes produced a dramatic effect on As concentrations in rice plants (P < 0.001; Figure 2a-c). Rice grown under continuously flooded conditions had the highest As concentrations and that under continuously aerobic conditions the lowest concentrations; the difference between these two treatments were 63-, 26-, and 20-fold for straw, husk, and grain As, respectively. In the aerobic-flooded treatment, As concentrations in all three parts of rice were approximately 80% lower than those of the continuously flooded treatment. Switching water management from flooded to aerobic at flowering decreased grain, straw, and husk As concentrations by 50, 44, and 35%, respectively, compared with the continuously flooded treatment. Inorganic As accounted for 40-100% of the total As concentration in the grain, with the remainder being DMA (Figure 2d; Supporting Information, Figure S3a). The perVOL. 43, NO. 10, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 1. Effects of water management regimes on soil redox potential (a), the concentration of arsenite (b) and arsenate (c) in soil solution, and the relationship between Eh and As mobilization (d). F ) flooded, A ) aerobic, F-A ) flooded-aerobic, A-F ) aerobic-flooded. Data are means ( SE (n ) 4).

FIGURE 2. Effects of water management regimes on total As concentration in straw (a), husk (b), and grain (c) and (d) As speciation in grain. Data are means ( SE (n ) 4). centage of total As present as inorganic As shows a pattern opposite to that of the total As concentration, increasing in the order flooded (42%) < flooded-aerobic (56%) < aerobic-flooded (89%) < aerobic (100%) (P < 0.001). Compared with the continuously flooded treatment, the concentration of inorganic As in grain was 87, 25, and 46% lower in the aerobic, flooded-aerobic, and aerobic-flooded treatments, respectively (P < 0.001) (Figure 2d). Silicon Fertilizer Experiment. In the -Si treatment, the Si concentration in the soil solution decreased from 6.2 mg L-1 on day 9 to 0.2-0.4 mg L-1 between days 45 and 121. The addition of Si fertilizer increased soil solution Si markedly (Figure 3a). The concentration of As in soil solution increased rapidly after day 23 and reached a plateau by day 72 (Figure 3b). Arsenite accounted for 78-100% of the total soluble As between days 23 and 121. The addition of Si fertilizer 3780

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significantly (P < 0.001) increased the concentrations of arsenite (days 45-121) and arsenate (days 72-99) in soil solution. The addition of Si increased grain and straw yield significantly (P e 0.001; Supporting Information, Figure S4 and Table S3). The concentration of Si in straw more than doubled with Si fertilization (Supporting Information, Figure S5). Silicon addition had a large effect (P < 0.001) on the total concentrations of As in straw and husk, decreasing their concentration by 78 and 50%, respectively (Figure 4a,b). The effect of Si on grain As concentration was significant (P < 0.05) but smaller (on average 16% decrease; Figure 4c). There was a significant (P < 0.01) cultivar difference in husk As concentration, but not in straw or grain As concentration. Arsenic speciation in rice husk and grain was significantly influenced by both genotype and Si treatment (Figure 4d,e;

FIGURE 3. Effects of Si fertilization on the dynamics of silicic acid (a) and arsenite and arsenate (b) in soil solution. Data are means ( SE (n ) 4). Supporting Information, Figure S6a). On average, the husk contained 64% inorganic As and 36% DMA. J7089 contained a higher percentage of inorganic As (74%) than J7091 (54%) (P < 0.001). Silicon fertilization markedly decreased the percentage of inorganic As in the husk, from 88% to 40% (P < 0.001) (Figure 4d). Grain contained proportionally more DMA and less inorganic As than the husk. J7089 had a larger percentage (49%) of inorganic As in grain than J7091 (36%) (P ) 0.003). The addition of Si fertilizer decreased the percentage of inorganic As from 56% to 29% (P < 0.001) (Supporting Information, Figure S6a), while there was no significant interaction between genotype and Si treatment. On average, for the two genotypes, Si addition decreased the concentration of inorganic As in grain by 59% (P < 0.001), but increased DMA by 33% (P < 0.05) (Figure 4e).

4. Discussion Water Management. Flooding of soil led to a marked mobilization of As, mainly arsenite, in the soil solution (Figure 1). This phenomenon has been well-documented and is attributed to a reductive dissolution of Fe oxides/hydroxides, which releases the sorbed As, and decreased adsorption of arsenite (11, 12, 17, 27). Therefore, the most effective way to mitigate the problem of excessive As accumulation in rice would be to grow rice aerobically throughout the entire season (Figure 2; also ref 12). However, while plant biomass and grain yield were broadly similar among the different water management regimes in our greenhouse experiment, continuous cultivation of aerobic rice results in a substantial yield decline, possibly because of the build-up of nematodes and soil pathogens under aerobic conditions (28, 29). One way to overcome this problem is to have periodic flooding and aerobic conditions. In fact, it is not uncommon that the standing water is drained from paddy fields during the grain filling stage. The present study shows that growing rice aerobically during either the vegetative (0-96 days) or the reproductive (97-147 days) stage substantially decreased As accumulation in rice straw, husk, and grain (Figure 2); the effect of the former was larger than that of the latter because of the longer period of aerobic conditions. It is clear that the soil redox potential had a decisive effect on the bioavailability of As to rice plants. In a similar principle, rice grown in special

raised beds of soil in paddy fields, which remain at higher redox potential, contained less As than conventional flooded rice (30). The fact that draining water after flowering decreased As concentrations in rice grain and husk compared with the continuously flooded treatment and that flooding after flowering increased As concentration in the rice tissues compared with the continuously aerobic treatment suggests that As in rice grain and husk was derived from both the uptake before and after flowering. Arsenic taken up by plants after flowering may reach rice grain mainly through xylem transport, whereas As taken up preflowering would have to be remobilized from stem and leaf tissues and transported via phloem to reach grain. The fact that postflowering uptake of As from soil contributed considerably to grain As accumulation explains why maintaining aerobic conditions in the later phase of rice growth helped decrease As concentration in grain. Water management significantly influenced the speciation of As in rice grain (Figure 2d). Because no methylated As was detected in the soil solution, DMA in rice grain must be synthesized in planta. Methylation of As was enhanced with increasing As concentration in the grain (Figure 2d; Supporting Information, Figure S3b); this is consistent with previous findings (2, 12, 31) and suggests that methylation may be a response to As stress in plants. Enhanced methylation in flooded-grown rice partly alleviates the risk of high As accumulation. Nevertheless, the concentration of inorganic As in grain was significantly decreased by aerobic management over all or a portion of rice growth duration (Figure 2d). Silicon Fertilization. Rice is a strong Si accumulator with straw Si concentration typically varying from 5 to 10% (32). Silicon is a beneficial element to rice as it enhances the resistance of rice plants against biotic and abiotic stresses, and Si fertilizers are used in many rice-growing areas (32, 33). The beneficial effect of Si on rice yield was also seen in our pot experiment. This effect was not due to Si decreasing the toxicity of As, because the plants did not suffer from As toxicity in the experiment. However, in more contaminated soils, Si may well alleviate As toxicity by decreasing As uptake (see below) and increasing stress resistance. In contrast to arsenate, which is taken up by phosphate transporters, arsenite is taken up by rice roots mainly through the Si uptake pathway (13). Results from the present study show that Si fertilization was highly effective in decreasing As accumulation in rice straw and husk and to a lesser extent, although still significantly, in rice grain (Figure 4). This inhibitory effect occurred even though the addition of Si (in the form of sparingly soluble SiO2 gel) significantly increased As concentration in the soil solution (Figure 3), presumably through a replacement of arsenite or arsenate adsorbed on Fe oxides/hydroxides by silicic acid. The inhibition of arsenite uptake by Si greatly outweighed the effect of an increased As availability in the soil. Si concentrations in the paddy soil solutions typically vary from 3 to 20 mg L-1 (32, 33). In comparison, the soil used in the pot experiments had a low Si availability (Figure 3), resulting in low Si concentrations in rice straw (Supporting Information, Figure S5). This low Si availability could explain the high As accumulation in rice from the soil used in the present study, which contains only a slightly elevated level of total As. River waters generally contain 4-16 mg L-1 dissolved Si, which, when used for irrigation, provide an important source of Si to rice crops (33). In comparison, well waters tend to contain lower levels of Si (33). Therefore, irrigation with shallow tube-well waters containing high As and low Si would be conducive to high As accumulation by rice. The inhibitory effect of Si was also reported when arsenate was the form supplied to rice plants in hydroponic experiVOL. 43, NO. 10, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 4. Effects of Si fertilization on total As concentration in straw (a), husk (b), and grain (c) and As speciation in husk (d) and grain (e) of two rice genotypes. Data are means ( SE (n ) 4).

ments, yet Si and arsenate did not compete for the same influx transporters (34). This observation can now be explained by the involvement of the efflux transporter Lsi2. Because arsenate is reduced rapidly to arsenite in rice roots, with arsenite being the main form transported in the xylem (16), Si is expected to inhibit arsenite efflux from root cells toward the xylem, which is mediated by Lsi2, and consequently As accumulation in rice shoots. Importantly, Si fertilization not only decreased As accumulation in rice shoots and grain but also influenced As speciation in grain by decreasing the concentration of inorganic As while increasing the concentration of DMA in both rice husk and grain (Figure 4). Thus, Si fertilization provides an attractive mitigation measure for decreasing As accumulation in rice, in addition to its beneficial effect on rice yield. Silicon fertilization had a much larger effect on inorganic As (-59%) than on the concentration of total As (-16%) in grain. The decrease in inorganic As can be explained by the competitive inhibition effect of Si on arsenite uptake and transport toward grain tissue. However, how Si enhances As methylation remains to be investigated. The negative relationship between percent inorganic As and total As concentration seen in the water management experiment (Supporting Information, Figure S3b) was not observed in the Si experiment (Supporting Information, Figure S6b), because both total As concentration and percent inorganic As were decreased by Si fertilization. In the Si fertilization experiment, a significant difference in As speciation in grain was found between two rice genotypes that accumulated similar concentrations of total As (Figure 4). This is consistent with an earlier report on genotypic variation in As speciation (35). It is clear from the present study that As methylation is influenced by both genetic and environmental (e.g., water management and Si availability) factors. In conclusion, the present study has demonstrated that water management, Si fertilization, and selection of rice cultivars had a profound effect on As accumulation and/or speciation in rice grain under greenhouse conditions. Further 3782

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research should be carried out to assess their efficacies on different soil types under field conditions.

Acknowledgments Rothamsted Research is an institute of UK Biotechnology and Biological Sciences Research Council. This project was partly funded by UK DFID-BBSRC grant BB/F004087/1. The work by J. F. Ma was supported by a Grant-in-Aid for Scientific Research on Priority Areas from the Ministry of Education, Culture, Sports, Science and Technology of Japan (No. 17078008).

Supporting Information Available Tables S1-S3 and Figures S1-S6. This material is available free of charge via the Internet at http://pubs.acs.org.

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