Effects of Water Management on Cadmium and Arsenic Accumulation

Nov 10, 2009 - Noriko Yamaguchi , Toshiaki Ohkura , Yoshio Takahashi , Yuji Maejima , and Tomohito Arao. Environmental Science & Technology 2014 48 (3...
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Environ. Sci. Technol. 2009 43, 9361–9367

Effects of Water Management on Cadmium and Arsenic Accumulation and Dimethylarsinic Acid Concentrations in Japanese Rice T O M O H I T O A R A O , * ,† A K I R A K A W A S A K I , † KOJI BABA,† SHINSUKE MORI,† AND SHINGO MATSUMOTO‡ National Institute for Agro-Environmental Sciences, Kannondai 3-1-3, Tsukuba, Ibaraki, 305-8604, Japan and Shimane University, Faculty of Life and Environmental Science, 2059 Kamihonjomachi, Matsue, Shimane, 690-1102, Japan

Received July 29, 2009. Revised manuscript received October 23, 2009. Accepted October 29, 2009.

Rice consumption is a major source of cadmium and arsenic for the population of Asia. We investigated the effects of water management in rice paddy on levels of cadmium and arsenic in Japanese rice grains. Flooding increased arsenic concentrations in rice grains, whereas aerobic treatment increased the concentration of cadmium. Flooding for 3 weeks before and after heading was most effective in reducing grain cadmium concentrations, but this treatment increased the arsenic concentration considerably, whereas aerobic treatment during the same period was effective in reducing arsenic concentrations but increased the cadmium concentration markedly. Flooding treatment after heading was found to be more effective than flooding treatment before heading in reducing rice grain cadmium without a concomitant increase in total arsenic levels, although it increased inorganic arsenic levels. Concentrations of dimethylarsinic acid (DMA) in grain were very low under aerobic conditions but increased under flooded conditions. DMA accounted for 3-52% of the total arsenic concentration in grain grown in soil with a lower arsenic concentration and 10-80% in soil with a higher arsenic concentration. A possible explanation for the accumulation of DMA in rice grains is that DMA translocates from shoots/roots to the grains more readily than does inorganic arsenic.

Introduction Cadmium (Cd) is toxic to humans at concentrations lower than those at which it is toxic to plants, because its effects on humans are cumulative (1). Soil pollution by Cd has been of public concern since the 1970s, when it was discovered that daily ingestion of rice (Oryza sativa L.) containing high levels of Cd is the main cause of itai-itai disease (2). A healthbased guidance value for Cd of 7 µg kg-1 bodyweight per week [the provisional tolerable weekly intake (PTWI)] has been established by the Joint Expert Committee on Food Additives (JECFA) of the Food and Agriculture Organization and the World Health Organization (3). The Food Safety Commission Secretariat of Japan has set a PTWI of 7 µg kg-1 * Corresponding author phone: (81) 298-38-8313; fax: (81) 29838-8199; e-mail: [email protected]. † National Institute for Agro-Environmental Sciences. ‡ Shimane University. 10.1021/es9022738 CCC: $40.75

Published on Web 11/10/2009

 2009 American Chemical Society

body weight per week for Cd (4). Recently, the European Food Safety Authority established a tolerable weekly intake for Cd of 2.5 µg kg-1 body weight (5). The weekly intake of Cd from foods in Japan in 2001 was estimated to be 4.1 µg kg-1 body weight, and about half the Cd intake from foods was from rice (6). A re-evaluation of Cd is scheduled for the 2010 meeting of the JECFA. A maximum concentration of 0.4 mg kg-1 for Cd in white rice grain has been adopted by the Codex Alimentarius Commission (7). Rice is a staple crop in Asia and is the principal source of dietary intake of Cd in the Japanese population; therefore, minimizing the intake of Cd from rice is an important health issue. When a paddy field is flooded and the soil is in a reducing condition, any Cd in the soil combines with sulfur (S) to form CdS, which has a low solubility in water. However, when the field is drained and the soil is in an oxidative condition, CdS is converted into CdSO4, which is soluble in water (8). This means that the solubility of Cd changes depending on the redox potential (Eh) of the soil (9). The Eh of paddy field soil can be controlled by means of water management, so it is possible to control Cd absorption by paddy rice through water management. Several studies conducted on the effects of water management on Cd absorption by paddy rice have confirmed that it is possible to control the Cd content of brown rice through water management during the growing period (10-12). Inahara et al. (12) reported that flooding paddy soil during the period from 15 days before heading (ear emergence) to 25 days after heading reduced the Cd concentration in brown rice to 0.08 mg kg-1; this represented a percentage reduction in Cd content of 84% compared with a control plot managed by intermittent irrigation. Arsenic (As) is a carcinogen and the intake of inorganic As in rice is a significant risk factor for cancer in populations for whom rice is a staple foodstuff (13). In some cases, human As intake from the consumption of rice exceeds that from drinking water (14). For inorganic As, a PTWI of 15 µg kg-1 body weight has been established by the JECFA (15). The Ministry of Agriculture, Forestry, and Fisheries of Japan analyzed the As contents of staple crops in Japan (16) and found that As concentrations in brown rice ranged from 0.04 to 0.33 mg kg-1, with an average value of 0.16 mg kg-1 (n ) 199); the average values for wheat, soybean, and spinach were 0.008, 0.005, and 0.010 mg kg-1, respectively. Rice is, therefore, a major source of dietary intake of inorganic As in the Japanese population. Contamination by As occurs to a greater extent in paddy rice than in other upland crops because anaerobic conditions in paddy soil lead to arsenite mobilization and, thus, enhanced bioavailability to rice (17). Maejima et al. (18) reported on As contamination in soils and crops in Japan and summarized investigations of As pollution in Japanese paddy fields. In the 1970s and 1980s, the mechanism of As damage to paddy rice and countermeasures for paddy rice fields were clarified by Koyama et al. (19) and Yamane et al. (20). Koyama et al. (19) conducted experiments with paddy rice grown in pots of As-contaminated soils and found a significant negative correlation between the yields of brown rice and the levels of 1 M HCl soluble As in the soil. The Japanese criterion for As pollution of paddy fields was set at 15 mg kg-1 of 1 M HCl soluble As so that the rice yield was not reduced by more than 10% (19). As-contaminated soils should be maintained in an oxidative state to suppress the dissolution of As (20, 21). A paddy field is considered to be in a safe oxidative state when free Fe(II) ions can be barely detected by the use of a 2,2′-dipyridyl indicator dye, which is a tool for confirming the presence of reducing conditions in soil (20). VOL. 43, NO. 24, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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As is present in rice grain both as inorganic As (mainly arsenite) and as dimethylarsinic acid [DMA; Me2As(O)OH] (14); inorganic As is generally considered to be more toxic than methylated As compounds (22). Xu et al. (21) reported that grain of aerobically grown rice contained As almost exclusively in the form of inorganic As, whereas in rice from flooded paddy, DMA accounted for the majority of the total As; methylation of As in rice may be a response to increased As loading in grains. Flooding of paddy fields is effective in reducing grain levels of Cd; however, anaerobic conditions in paddy soil lead to arsenic mobilization and, therefore, As uptake by rice could increase (19). The main objective of the present study was to investigate the simultaneous effects on Cd and As levels in rice grains induced by water management of paddy soil before and after emergence of the rice ears. We also investigated the speciation of As in rice grains under flooded and aerobic paddy conditions.

Materials and Methods Pot Experiments. Pot experiments, with three or six (treatment 1) replications each, were performed in 2008 in a greenhouse at ambient temperatures (7-36 °C) under sunlight. Wagner pots (1/5000 a, Fujiwara Scientific Co., Tokyo, Japan) were filled with 3 kg of two kinds of soil collected from the plow layer of paddy fields. Soil A contained 1.6% total C, 0.15% total N, 0.56 mg kg-1 total Cd, and 25 mg kg-1 total As, and it had a pH of 5.6. Soil B contained 3.4% total C, 0.32% total N, 0.66 mg kg-1 total Cd, and 48 mg kg-1 total As, and it had a pH of 5.5. Eh was measured at a depth of 10 cm. A soil-water sampler (DIK8393, Daiki Rika Kogyo Co., Saitama, Japan) was buried in the middle of the soil of each pot for collecting soil solution. The soil solution was sampled 33, 54, 70, 83, and 90 days after transplanting and diluted with 10% HNO3 at a ratio of 9:1 immediately after collection and filtered through a sterilized 0.45 µm filter. Seedlings of rice (O. sativa L. cv. Koshihikari) were germinated on perlite and transplanted into the soil samples on 14 May 2008. A compound fertilizer containing 0.2 g of N, 0.04 g of P, and 0.08 g of K was supplied to each pot by basal application. Ammonium sulfate containing 0.2 g of N was also supplied to each pot by top dressing 60 days after transplantation of the rice seedlings. Seven water-management treatments were examined in the experiment: treatment 1 involved flooding throughout the entire growth period; treatment 2, flooding from transplanting to 3 weeks after heading; treatment 3, flooding from transplanting to heading; treatment 4, flooding from transplanting to 3 weeks before heading and from heading to 3 weeks after heading; treatment 5, flooding from transplanting to 3 weeks before heading; treatment 6, flooding from transplanting for 2 weeks and then from 3 weeks before heading to 3 weeks after heading; and treatment 7, flooding from transplanting for 2 weeks. The heading days occurred between August first and August sixth. Water management was changed at the beginning of the last heading day of each treatment of the pot experiments. At the time of heading in treatment 1, the stems of the plants grown in three pots were cut 2 cm above the soil surface and the xylem sap that exuded from the cut surface was collected by trapping in a 1.5 mL plastic vial containing a small piece of cotton for 2 h after cutting the shoots (23). After the seeds had matured, the plants were cut off at the stem above the point at which they were immersed in water. Chemical Analysis of Plant Tissues and Statistical Methods. Husks and unfilled grains were removed, and the filled grains and the straw were oven-dried at 75 °C. The grains and straw samples were each ground to a fine powder, and 0.5 g samples were digested in 5:1 (v/v) HNO3/H2O2 (5 9362

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mL) in a microwave oven (MLS 1200, Milestone, FKV, Italy) (24). Concentrations of Cd and As in the digested samples, soil solution, and xylem sap were determined by inductively coupled plasma (ICP)-optical emission spectroscopy (VistaPRO, Varian, Inc., Palo Alto, CA,) and ICP-mass spectrometry (ICP-MS) (ELAN DRC-e, Perkin-Elmer Sciex, DE). Accuracy was evaluated by the use of a certified reference material (rice flour, NMIJ CRM 7502-a No.7 Cd Level II). To determine As speciation in rice grain, a powdered sample of ground rice (0.5 g dry weight) was mixed with 2 mL of HNO3 (0.15 M) in a 10 mL capped high-density polyethylene centrifuge tube, and the mixture was heated on an aluminum heating block at 80 °C for 2 h. The solution obtained was diluted to 10 mL with water and passed through a 0.45 µm filter before analysis (25). For As speciation of rice straw, ears, and stems and leaves, 5 mL of 68% aqueous HNO3 was added to a ground powder sample (0.5 g dry weight) in a 50 mL Teflon tube, and the mixture was heated at 100 °C for 4 h. The solution obtained was diluted to 50 mL with water and passed through a 0.45 µm filter before analysis (26). The As speciation in the grain, straw, ear, stems and leaves, and xylem sap of rice and in the soil solution were determined by HPLC/ICP-MS [PU 712i (GL Science, Tokyo, Japan); ELAN DRC-e] (26). HPLC/ICP-MS analysis showed that the rice grain samples contained mostly arsenite and DMA, with trace amounts of arsenate. However, because HNO3 is generally regarded as an oxidative acid (25), the sum of arsenite and arsenate was presented as the total inorganic As. The Student’s t-test and the least-significant difference (LSD) test were used to test for statistical significance in differences between treatments.

Results Soil Redox Potential. In treatments 1, 2, 3, 4, and 5 in soil A, the redox potential (Eh) of the soil decreased and fell to below -200 mV 55 days after flooding (Figure S1 in the Supporting Information). In treatments 1, 2, 3, 4, and 5 in soil B, the value of Eh fell to below -200 mV less than 13 days after flooding. In treatments 2, 3, 4, and 5, the value of Eh increased again immediately after aerobic treatment. In treatment 7, the value of Eh in both soils fluctuated more than in the other treatments 55 days after transplantation under aerobic conditions; in some pots, excess soil-water reduced the value of Eh in treatment 7, but the mean Eh of three pots remained above 0 mV under aerobic conditions. This could be due to low transpiration of the rice plants in treatment 7, because the rice plants subjected to treatment 7 grew less well than those subjected to the other treatments (Figure S2 in the Supporting Information). As Concentrations and As Speciation in Soil Solution. The total As concentration in the soil solution in soil A increased until day 70 in treatments 1, 2, and 3 and remained at elevated levels in treatments 1 and 2 but decreased in the aerobic phase of treatment 3 on day 83 (Figure 1). Total As concentrations in the soil solution in soil A increased until day 54 in treatments 4 and 5 and then decreased on day 70. In treatment 5, the total As concentrations in soil solution remained at low levels on days 83 and 97. In treatment 4, the total As concentrations in the soil solution in soil A remained at low levels on day 83 but increased on day 97. The total As concentrations in the soil solution in soil A on days 33 and 54 were low under aerobic conditions from day 14 to day 58 after transplantation (treatments 6 and 7), and these remained at a low level in the case of treatment 7 but increased in treatment 6 on days 70, 83, and 97. The total As concentrations in the soil solution in soil B on days 33 and 54 were high under flooded conditions from day 0 to 58 after transplanting (treatments 1, 2, 3, 4, and 5), and these remained at an elevated level in treatments 1, 2,

FIGURE 1. Effects of water management on As and Cd concentrations in soil solution. The plotted points are mean values ( SE (n ) 3). Total Cd concentrations in the soil solution of both soils were below detection limits throughout the entire growth period in treatments 1 and 2. VOL. 43, NO. 24, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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a

Mean values ( SE (n ) 3); sum As ) inorganic As + DMA (sum As/total As %). Results followed by the same letter are not significant at the 5% level.

0.010 ( 0.003 a 0.046 ( 0.011 b 0.27 ( 0.012 d 0.16 ( 0.011 c 0.34 ( 0.020 e 0.063 ( 0.006 b 0.38 ( 0.011 e 1.4 ( 0.073 a 1.1 ( 0.125 b 0.38 ( 0.014 d 0.23 ( 0.014 d 0.03 ( 0.002 e 0.79 ( 0.060 c 0.01 ( 0.001 e 0.35 ( 0.034 ab 0.30 ( 0.022 b 0.15 ( 0.014 c 0.36 ( 0.018 ab 0.11 ( 0.007 c 0.39 ( 0.011 a 0.10 ( 0.009 c 1.7 (100) 1.4 (83) 0.53 (90) 0.59 (100) 0.14 (83) 1.17 (93) 0.11 (82) 1.7 ( 0.118 a 1.7 ( 0.077 a 0.59 ( 0.014 c 0.60 ( 0.037 c 0.17 ( 0.030 d 1.26 ( 0.044 b 0.14 ( 0.027 d 0.005 ( 0.001 a 0.016 ( 0.002 a 0.36 ( 0.003 d 0.21 ( 0.018 b 0.41 ( 0.034 e 0.066 ( 0.006 a 0.28 ( 0.021 c 0.48 ( 0.044 a 0.37 ( 0.021 b 0.09 ( 0.006 c 0.08 ( 0.009 c 0.003 ( 0.003 d 0.14 ( 0.011 c 0.01 ( 0.006 d 0.93 (97) 0.79 (87) 0.31 (101) 0.41 (113) 0.11 (107) 0.63 (114) 0.13 (120) 0.95 ( 0.044 a 0.92 ( 0.029 a 0.30 ( 0.020 c 0.36 ( 0.007 c 0.11 ( 0.026 d 0.55 ( 0.006 b 0.10 ( 0.014 d 1 2 3 4 5 6 7

0.45 ( 0.028 a 0.42 ( 0.027 a 0.22 ( 0.020 c 0.32 ( 0.028 b 0.11 ( 0.007 d 0.49 ( 0.036 a 0.12 ( 0.012 d

Cd (mg kg-1) DMA (mg kg-1) Inorganic As (mg kg-1) sum As (mg kg-1) total As (mg kg-1) water management

Inorganic As (mg kg-1)

DMA (mg kg-1)

Cd (mg kg-1)

total As (mg kg-1)

sum As (mg kg-1)

soil B soil A

TABLE 1. Effects of Water Management on As Speciation and Cd Concentration in Graina

and 3 but decreased in the aerobic treatments 4 and 5 on day 70 (Figure 1). In treatment 5, the total As concentrations in the soil solution in soil B remained at a low level on days 83 and 97. In treatment 4, the total As concentrations in the soil solution in soil B remained at a low level on day 83 but increased on day 97. In treatment 3, the total As concentrations in the soil solution in soil B remained at a high level on day 83 but decreased rapidly on day 97. The total As concentrations in the soil solution in soil B on days 33 and 54 were low under aerobic conditions from day 14 to 58 after transplantation (treatments 6 and 7), and they remained at a low level in treatment 7 but increased in treatment 6 on days 70, 83, and 97. The DMA concentration in the soil solution was 2.8-fold higher in soil B than in soil A at the time of heading in treatment 1 (Table 2). Cd Concentration in Soil Solution. Total Cd concentrations in the soil solution of both soils were below detection limits throughout the entire growth period in treatments 1 and 2. The total Cd concentrations in soil solution of both soils on days 33 and 54 remained below detection limits in treatments 3, 4, and 5 (Figure 1) but increased in aerobic treatments 4 and 5 on day 70. In treatment 5, the total Cd concentrations in the soil solution of both soils increased on days 83 and 97. In treatment 4, the total Cd concentrations in the soil solution of soil B increased on day 83 but decreased on day 97. In treatment 3, the total Cd concentrations in the soil solution of both soils increased on day 97. The total Cd concentrations in soil solutions of both soils on day 33 and 54 were high under aerobic conditions from day 14 to day 58 after transplantation (treatments 6 and 7, Figure 1), and they remained at a high level in treatment 7 but decreased in treatment 6 on days 70, 83, and 97. Cd and As Concentrations and As Speciation in Plants. Yields of rice grain and straw were significantly different for the various water treatments and were highest for the continuous flooding treatment 1 and lowest for the aerobic treatment 7 (Figure S2 in the Supporting Information). In both the soils, rice from the continuous flooding treatment 1 had the lowest Cd concentration and the highest As concentration in grain (Table 1). Rice from treatment 5 had the highest Cd concentration in grain in soil A, and rice from treatments 5 and 7 had higher Cd concentrations in grain than rice from other treatments in soil B; rice grains from treatments 5 and 7 also had the lowest As concentration in both. The As concentrations in grain were significantly different between treatment 1 and treatment 2 in both soils. In both soils, rice grain from treatment 6, where flooded conditions existed between 3 weeks before heading and 3 weeks after heading, had a higher concentration of As and a lower concentration of Cd than rice grain from treatments 3, 4, 5, and 7. Rice grain from treatment 4 had a 59-62% lower Cd concentration than that from treatment 3 in both soils; however, the As concentrations in the rice grains were not significantly different between treatments 3 and 4 in both soils. DMA concentrations in grain were very low in treatments 5 and 7 in both soils. Under flooded conditions, the proportion of DMA to total As in grain increased in both soils and reached values of 52% and 80% in treatment 1 in soils A and B, respectively. In soils A and B, rice straw from the continuous flooding treatments 1 and 2 had a higher As concentration and a lower Cd concentration than rice straw from other treatments (Table S1 in the Supporting Information). Rice straw from treatment 4 had a significantly lower Cd concentration than rice straw from treatment 3 in both soils. Rice straw from treatment 4 also had a significantly lower As concentration

TABLE 2. As Speciation in Soil Solution, Xylem Sap, Stems and Leaves, Ears (Treatment 1, 76 Days), and Straw (Treatment 1, Harvesting Time)a soil solution (mg L-1)

xylem sap (mg L-1)

soil A soil B

0.004 ( 0.0002 * 0.011 ( 0.0002 *

0.007 ( 0.003 * 0.037 ( 0.005 *

soil A soil B

0.18 ( 0.003 * 0.38 ( 0.062 *

0.14 ( 0.075 0.16 ( 0.015

stems and leaves (mg kg-1) DMA BD 1.3 ( 0.1 Inorganic As 4.7 ( 0.4 * 7.8 ( 0.2 *

ears (mg kg-1)

straw (mg kg-1)

0.13 ( 0.03 * 1.1 ( 0.03 *

0.4 ( 0.16 * 1.0 ( 0.12 *

0.57 ( 0.11 0.63 ( 0.09

21.4 ( 0.7 24.1 ( 2.5

a Data are mean ( SE (n ) 3). BD: below detection limits. Significant differences as determined by Student’s t-test are indicated by * (P ) 0.01)

than rice straw from treatment 3 in soil A. Rice straw from the aerobic treatment 7 had the lowest As concentration in both soils. The DMA concentration in the xylem sap was 5.3-fold higher in soil B than in soil A, whereas the DMA concentration in stems and leaves was below detection limits in soil A and was 1.3 mg kg-1 in soil B (Table 2). The DMA concentration in ears was 8.5-fold higher in soil B than in soil A. The inorganic As concentration in the soil solution was 2.1-fold higher in soil B than in soil A. The inorganic As concentration in the xylem sap was 1.1-fold higher in soil B than in soil A, and the inorganic As concentration in stems and leaves was 1.7-fold higher in soil B than in soil A. The inorganic As concentration in ears was 1.1-fold higher in soil B than in soil A. At the time of harvesting in treatment 1, the DMA concentration in straw was 2.3-fold higher in soil B than in soil A, whereas the inorganic As concentration in straw was not significantly different between soil B and soil A.

Discussion Flooding treatment increased the concentration of As in rice grain and straw, whereas aerobic treatment increased the concentration of Cd in rice grain and straw (Table 1 and Table S2 in the Supporting Information). This occurs because flooding decreases the redox potential of the soil and increases the As concentration in the soil solution, whereas aerobic treatment increases the redox potential of the soil and increases the Cd concentration in the soil solution (Figure S2 in the Supporting Information and Figure 1). For reducing the Cd concentration in grain, flooding 3 weeks before and after heading (treatments 1, 2, and 6) was most effective; however, the As concentration in grain increased considerably as a result. On the other hand, for reducing the As concentration in grain, aerobic treatment for 3 weeks before and after heading (treatments 5 and 7) was most effective, but the concentration of Cd in the grain increased considerably as a result. Flooding for 3 weeks after heading was more effective in reducing Cd concentrations in grain than was flooding for 3 weeks before heading (Table 1); the effects on the As concentration in grain were similar for flooding 3 weeks after heading and for flooding for 3 weeks before heading. The value of Eh increased to above 0 mV immediately after aerobic treatment in treatment 3, and the Cd concentrations in the soil solutions of both soils on day 97 in treatment 4 were below detectable limits (Figure 1 and Figure S1 in the Supporting Information). However, the value of Eh gradually decreased and fell below -200 mV about 100 days after flooding in treatment 4 (Figure S1 in the Supporting Information). Therefore, the uptake of Cd by rice from the soil solution should increase immediately after the aerobic treatment of treatment 3, and the uptake of As by rice from the soil solution should not increase immediately after the flooding treatment of treatment 4. The effect of flooding

treatment after heading on the accumulation of Cd by rice grain should be greater than that on accumulation of As. Levels of inorganic As in grain were much higher in treatment 4 than in treatment 5 or treatment 3. Therefore, flooding after heading should produce a greater increase in inorganic As levels than flooding before heading. Because As accumulation in grain should be greater after heading than before heading, flooding after heading should lead to arsenic mobilization in soil and, thus, grain levels of inorganic As should increase. Another possibility is that the relocation of As from the leaves increases. Grain As concentrations in treatments 5 and 7 were almost the same (Table 1), so flooding until day 52 after transplanting did not affect the grain As concentrations when rice was grown in aerobic conditions after day 52. The grain As concentrations in treatment 1 were 1.2-fold higher than those in treatment 2 in both soils, whereas grain Cd concentrations in treatment 2 were 2.3- and 4.7-fold higher than in treatment 1 in soil A and soil B, respectively (Table 1). Therefore, water management just before harvesting time should have a greater impact on the Cd concentration in grain than on the As concentration. The same water-management regime could cause different changes in the redox potentials for various types of soils because of differences in the properties of the soils, such as aggregate development. It may, therefore, be difficult to maintain low Cd and As concentrations in grain simultaneously by means of water management alone. Silicon fertilization decreases As and Cd concentrations in rice grain (27, 28), so it will be necessary to screen for more materials that could reduce As and/or Cd concentrations in rice grain. Some tropical japonica cultivars with low levels of As in their grains have the potential to be used in breeding (29). The As concentration in the soil solution of soil B was much higher than that in the soil solution of soil A under flooded conditions (Figure 1); however, the concentrations of As in straw were similar for both soils (Table S1 in the Supporting Information). Although the total As concentrations were higher in grain grown in soil B than for grain grown in soil A, the inorganic As concentration was similar between the soils for the same water-management regime (Table 1). On the other hand, the straw DMA concentration was 2.3-fold higher in soil B than in soil A. Raab et al. (30) reported that rice translocates DMA very efficiently into shoots. Shoot-to-root transfer factors for two rice varieties, Azucena and Balawere, were 0.02 and 0.01 to arsenate, respectively, and 0.87 and 0.11 to DMA, respectively. The DMA concentration in the xylem sap was 1.8- to 3.4-fold higher than in the soil solution, whereas the inorganic As concentration in the xylem sap was 0.4- to 0.8-fold lower than in the soil solution (Table 1). Therefore, rice var. Koshihikari can translocate DMA efficiently into its shoots. Most of the inorganic As could have been accumulated in the roots, and translocation from roots to shoots was similar in both soils. However, DMA translocation from roots to VOL. 43, NO. 24, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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shoots was higher in soil B than in soil A, because the level of DMA in the soil solution was higher in soil B than soil A. At the heading stage, the DMA concentration in stems and leaves of rice grown in soil B was high, whereas no DMA was detected in stems and leaves of rice grown in soil A; however, DMA concentrations in ears of rice grown in both soils were high. Because the inorganic As concentration in the ears was similar in soil A and in soil B, it is unlikely that As methylation activity could be induced by inorganic As in ears grown in soil B only. Soluble organic As concentrations in soil are high under reducing conditions (31). Twenty-one days after transplanting, the soil redox potential in treatments 1 and 2 in soil B were already below -200 mV, whereas in treatments 1 and 2 in soil A, the soil redox potential did not fall below -200 mV until 55 days after transplantation (Figure S1 in the Supporting Information). So DMA levels in soil solution from transplantation to 55 days after transplantation were lower in soil A than in soil B. As is transported from the roots to the ears after day 55, because the panicle-formation stage of rice begins about 3 weeks before the heading time. For this reason, although levels of DMA were below detection limits in stems and leaves of rice grown in soil A, DMA was detected in the ears of rice grown in soil A. Xu et al. (21) reported that accumulation of As in rice grain increased markedly under flooded conditions; As concentrations in grain were 10- to 15-fold higher in rice grown under flooded conditions than in aerobically grown rice, and the proportion of DMA increased. We found that DMA accounted for 3-52% of the total As concentration in grain for soil A and 10-80% for soil B (Table 1). One possible explanation for the greater percentage of DMA in grain is that DMA translocates from shoots and roots to grain more easily than does inorganic As. Levels of DMA in ears grown in soil B were 8-fold higher than for those grown in soil A. These results suggest that different DMA concentrations in grains grown in soil A and soil B could be due to different amounts of DMA translocating from the roots. Another possible explanation is that DMA in rice grain is synthesized in planta (21). In conclusion, our study showed that water management before and after the heading time is important in managing the Cd and As concentrations simultaneously in rice grain. Further investigation is required to determine whether differences in the translocation of DMA from shoots and roots to grains or whether the induction of methyltransferase activity of DMA in rice is responsible for the increased DMA concentrations in grains.

Acknowledgments This work was supported by a grant from the Ministry of Agriculture, Forestry, and Fisheries of Japan (research project for ensuring food safety from farm to table AC-1122).

(4)

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(6) (7)

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(15) (16)

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Supporting Information Available Information on soil redox potential, straw and grain yield, and As and Cd concentrations in straw is available. This material is available free of charge via the Internet at http:// pubs.acs.org.

Literature Cited (1) Singh, B. R.; McLaughlin, M. J. Cadmium in soils and plants: summary and research perspective. In Cadmium in Soils and Plants; McLaughlin, M. J., Singh, B. R., Eds.; Kluwer Academic Publishing: Dordrecht, 1999; pp 257-267. (2) Kobayashi, J. Pollution by cadmium and the itai-itai disease in Japan. In Toxicity of Heavy Metals in the Environment; Oeheme, F. W., Ed.; Marcel Dekker: New York, 1978; pp 199-260. (3) Joint FAO/WHO Expert Committee on Food Additives: Evaluation of Certain Food Additives and Contaminants. Sixty-First Report of the Joint FAO/WHO Expert Committee on Food Additives; 9366

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