Phytoextraction by a High-Cd-Accumulating Rice - American Chemical

Jul 3, 2008 - Experiment Station, Akita Prefectural Agriculture, Forestry and Fisheries Research Center, Genpachisawa 34-1,. Yuwaaikawa, Akita, Akita ...
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Environ. Sci. Technol. 2008, 42, 6167–6172

Phytoextraction by a High-Cd-Accumulating Rice: Reduction of Cd Content of Soybean Seeds M A S A H A R U M U R A K A M I , * ,† N O R I H A R U A E , †,| S A T O R U I S H I K A W A , † TOSHIYUKI IBARAKI,‡ AND MASASHI ITO§ Soil Environment Division, National Institute for Agro-Environmental Sciences, 3-1-3, Kannondai, Tsukuba, Ibaraki 305-8604, Japan, Department of Soil and Environment, Fukuoka Agricultural Research Center, 587, Yoshigi, Chikushino, Fukuoka 818-8549, Japan, and Department of Production and Environment, Agricultural Experiment Station, Akita Prefectural Agriculture, Forestry and Fisheries Research Center, Genpachisawa 34-1, Yuwaaikawa, Akita, Akita 010-1231, Japan

Received January 16, 2008. Revised manuscript received May 6, 2008. Accepted May 28, 2008.

Soybeans (Glycine max (L.) Merr.) are the major summer crop grown in Japanese upland fields (characterized by aerobic soil) that have been converted from paddies. To evaluate the effect of phytoextraction by rice on the seed cadmium (Cd) content of soybeans grown subsequently, we grew Milyang 23, a highCd-accumulating rice cultivar, and then grew soybeans in three paddy soils contaminated with moderate Cd concentrations (2.50-4.27 mg Cd kg-1). The rice accumulated 7-14% of the total soil Cd in its shoots. The soybean seed Cd contents were 24-46% less than those grown on control soils. Phytoextraction by Milyang 23 rice is thus a promising remediation method for reducing seed Cd contents of soybeans grown on paddy soils under aerobic soil conditions.

Introduction Cadmium (Cd) is bioavailable through the food chain and is toxic to humans (1). The Codex Alimentarius Commission set maximum levels for Cd in wheat, potatoes, many vegetables (2), and polished rice (3). On the other hand, it discontinued work on developing a maximum level for Cd in soybeans, which it considered not to be a major contributor to Cd intake (4). However, soybeans are a major summer crop in Japan and, via tofu, natto, and soy sauce, are the main source of dietary intake of Cd in Japan (5). Thus, decreasing the Cd content of soybean seeds is extremely important. Engineering-based remediation methods such as soil excavation and landfilling are environmentally disruptive, limited to relatively small areas, and potentially expensive * Corresponding author phone and fax: +81-29-838-8313; e-mail: [email protected]. † National Institute for Agro-Environmental Sciences. ‡ Fukuoka Agricultural Research Center. § Akita Prefectural Agriculture, Forestry and Fisheries Research Center. | Present address: Graduate School of Agricultural Science, Kobe University, 1-1 Rokkodai, Nada, Kobe, Hyogo 657-8501, Japan. 10.1021/es8001597 CCC: $40.75

Published on Web 07/03/2008

 2008 American Chemical Society

(6). Hyperaccumulator-based phytoextraction is proposed as a low-cost amelioration technology (7, 8). However, hyperaccumulator plants pose difficulties in harvesting mechanically and in weed control and are prone to diseases prevailing in warm, humid weather (9–12). Large-scale phytoextraction by hyperaccumulators may thus not be an efficient remediation technology for monsoonal Asian fields with low to moderate Cd contamination. To maximize phytoextraction efficiency, it is important to select a phytoextractor species that is compatible with mechanized cultivation techniques and local climatic conditions. Such a plant may produce better results than one selected solely for its high tolerance to metal. Several phytoextraction studies have tested nonhyperaccumulator high-biomass plants such as Indian mustard (Brassica juncea L.; 9, 13), tobacco (Nicotiana tabacum L.; (14)), industrial hemp (Cannabis sativa L.; (15)), flax (Linum usitatissimum L.; (16)), vetiver grass (Vetiveria zizanioides; (17)), poplar (Populus spp.; (18)), and willow (Salix spp. (19)). These plants are cultivable in agricultural fields in Japan. However, rice (Oryza sativa L.) is the biggest crop in Japan, and its cultivation system is well-established and highly mechanized. In a previous study, we selected “Milyang 23” rice as a promising cultivar for the phytoextraction of Cd in paddy soils with low to moderate contamination (20). However, its effect on the Cd content of subsequently grown soybean seeds has not been reported. The Cd contents in soybean tissues and seeds at harvest were found to be directly related to soil Cd measured by a single extraction with 0.1 mol L-1 HCl (21). In contrast, sequential extraction provides detailed information such as the origin, mode of occurrence, and bioavailability of metals (22, 23). In a previous study, we found that soybean and rice decreased the exchangeable, inorganically bound, and organically bound Cd fractions, and the HCl-extractable Cd equaled 79-97% of the sum of these three fractions. Thus, HCl extraction, which is simpler and less expensive than the sequential and total extraction methods, is a useful diagnostic measure for evaluating the decrease in soil Cd concentration due to phytoextraction (20). Thus, it is necessary to assess the effects of the phytoextractor on mobilizing and depleting several metal fractions in addition to the metal concentrations of succeeding crops. The purpose of this study was to evaluate the potential of Milyang 23 rice for removing Cd from three paddy soils moderately contaminated with Cd, and the effects on the seed Cd concentrations of soybeans subsequently grown on those soils.

Materials and Methods Pot Experiment. In the first year, we grew rice in 1/600-a pots (surface area, 1661 cm2; depth, 30 cm) containing industrially contaminated paddy soils under aerobic soil conditions. The soils were collected from the top 15 cm of three paddy fields with moderate concentrations of Cd (an Andisol and two Entisols; (24)). The physicochemical properties of the soils are given in Table 1. The main sources of Cd appear to be wastewater from abandoned mines used for irrigation (Andisol and Entisol 2) and the atmospheric deposition of soot from a zinc refinery (Entisol 1). Each soil was air-dried, crushed, and passed through an 8-mm sieve by a rotary crusher with a stainless steel sieve (RKM-81E, Ishii Factory, Yamagata, Japan) and thoroughly mixed; 25 L was placed in each pot (19.6 kg of Andisol, 28.4 kg of Entisol 1, and 30.9 kg of Entisol 2). Basal fertilizer was supplied at 2.5 g N (as (NH4)2SO4), 1.1 g P (as single superphosphate), and 1.5 g K (as K2SO4) per pot. VOL. 42, NO. 16, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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TABLE 1. Selected Physico-Chemical Properties of the Soils Used in This Study soil source of contamination classificationa clay content (g kg-1) texture bulk density (g cm-3) pH (H2O) total C (g kg-1) total N (g kg-1) total Cd (mg kg-1) total Cu (mg kg-1) total Pb (mg kg-1) total Zn (mg kg-1) a

Andisol

Entisol 1

Entisol 2

wastewater from abandoned copper mine hydric melanudands 164 clay loam 0.78 6.03 66.3 5.4 4.27 96.6 157.4 195.8

atmospheric deposition of soot from zinc refinery typic fluvaquents 157 sandy clay loam 1.13 5.40 20.2 1.4 2.71 18.6 51.9 357.0

wastewater from abandoned copper mine typic fluvaquents 180 clay loam 1.23 5.50 24.2 1.8 2.50 45.6 33.5 352.7

Keys to soil taxonomy (24).

We grew Milyang 23 rice (Oryza sativa L.) as the phytoextractor (20). We sowed three seeds at each of 16 spots at intervals of 10 cm in each pot. The plants were grown in a greenhouse under natural light at ambient temperatures (18-30 °C) from May to October. The experiment used a randomized block design with three replicates. Pots were watered daily to maintain the soil-water content at near field capacity. Leachates after watering were not recovered. At 130 days after sowing, we harvested the shoots by cutting the stems approximately 5 cm above the soil. We then carefully removed the roots (with the residual stems) from the soil and air-dried all the soil from each pot separately. In the second year, we grew soybeans in 1/5000-a Wagner pots containing the phytoextracted soils or control (unphytoextracted and unwatered) soils under aerobic soil conditions. The soils were passed through a stainless steel 8 mm sieve and thoroughly mixed; then, 2.5 L was placed in each pot (2.0 kg of Andisol, 2.8 kg of Entisol 1, and 3.1 kg of Entisol 2). Roots of one rice plant (2.5 g) were added to each pot containing phytoextracted soil, since roots are left behind in the field. The pH values of the phytoextracted soils were 5.95 (Andisol), 5.33 (Entisol 1), and 5.38 (Entisol 2), which were not significantly different from those of control soils (see the Supporting Information, Figure S1). Liming is a prerequisite for increasing soybean yields on acidic soils (25). Suitable soil pH values for optimizing soybean yields are 6.0 to 6.5 (26). So before soybean culture, the pH values of the control and phytoextracted Entisols were raised to 6.0 by the addition of lime (CaCO3) according to the buffer curve method (27). Basal fertilizer was supplied as before at 0.16 g N, 0.26 g P, 0.25 g K, and 2 g CaMg(CO3)2 per pot. We grew Enrei and Suzuyutaka soybeans (Glycine max (L.) Merr.) as cultivars that accumulate low and high amounts, respectively, of Cd in their seeds (5). We sowed three seeds per pot and then thinned the seedlings to one per pot at 21 days after sowing. The plants were grown in a greenhouse under natural light at ambient temperatures (18-30 °C) from June to September. The experiment used a randomized block design with three replicates per treatment. Pots were watered daily to maintain the soil-water content at near field capacity. At maturity, 100 days after sowing, we harvested the seeds. Soil and Plant Analyses. We measured the soil pH and total soil C and N and soil Cd concentrations of seven fractions (0.01 or 0.1 mol L-1 HCl extractable Cd, exchangeable Cd, inorganically bound Cd, organically bound Cd, oxideoccluded Cd, and residual Cd), and dry weights (DWs) and Cd concentrations of harvested shoots and roots of rice and seeds of soybeans. Cd is known to interact with several elements in the metal uptake (28). Thus, we also measured the copper (Cu), lead (Pb), and zinc (Zn) concentrations in soils and plants. The methods of soil and plant analyses are detailed in the Supporting Information. 6168

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We performed several statistical analyses with Excel Tokei software (Esumi, Tokyo, Japan). Treatments were compared by Bonferroni’s multiple-comparison test and Student’s t-test. For Cd in rice, we analyzed the correlations between the soil Cd concentrations of seven extraction fractions plus their total from the control soils and the corresponding values of shoot and total Cd uptakes by Milyang 23. To derive regression equations for predicting shoot and total Cd uptakes from soil Cd concentrations, we performed regression analyses on the assumption that each regression line crossed the origin (x, y ) 0, 0) because, if there is no Cd in the soil, there will be no Cd in the plant. For Cd in soybeans, we analyzed the correlation between the soil Cd concentrations of the same seven fractions plus their total from the control and phytoextracted soils and the corresponding seed Cd concentrations in Enrei and Suzuyutaka soybeans. To derive regression equations for predicting seed Cd concentrations from soil Cd concentrations, we performed regression analyses on the same assumption as above. We evaluated the performance of each regression equation from the coefficient of determination (R2) and the significance by analysis of variance (ANOVA).

Results Cd in Shoots and Roots of Phytoextractor. The DW of, Cd concentration ([Cd]) in, and Cd uptake by shoots and roots of Milyang 23 rice are shown in Figure 1. The DWs of both shoots and roots were not significantly different among the three soils. No symptoms of toxicity were found in any plant. Both the [Cd] and the Cd uptakes decreased in the order Entisol 2 > Entisol 1 > Andisol in shoots and Entisol 2 ) Entisol 1 > Andisol in roots. Roots extended into the bottom of each pot (15 cm below soil surface). To present results comparable to field phytoextraction results, we converted the pot-basis data of the DWs and the Cd uptakes into per-hectare basis data (the right y axes of Figure 1). The converted shoot DW in Entisol 1 was 1.4 times the average value in the Entisol 1 field (Murakami et al., unpublished). Better growth conditions in the greenhouse than in the field would explain this increase. These indicate that it would need at least 1.4 times the phytoextraction in the field to obtain the same results as in this pot experiment. Cd Concentrations in Phytoextracted and Control Soils. The phytoextracted soils had significantly less Cd than the control soils in most fractions (Figure 2): exchangeable (P < 0.01; 23% less in Andisol, 31% in Entisol 1, and 14% in Entisol 2), inorganically bound (P < 0.01; 13%, 18%, and 28%), organically bound (P < 0.05; 8%, 10%, and 21%), 0.01 mol L-1 HCl-extractable (P < 0.05; 28%, 32%, and 42%), 0.1 mol L-1 HCl-extractable (P < 0.01; 13%, 23%, and 22%), and total (P < 0.01; 10%, 15%, and 19%). There were no significant differences in oxide or residual fractions in any soil.

FIGURE 1. Dry weights of (upper), Cd concentrations in (middle), and Cd uptakes by (lower) shoots (left) and roots (right) of Milyang 23 rice grown on three soils. Means in the same group with the same letter are not significantly different at P < 0.05 by Bonferroni’s multiple-comparison test. Error bars show standard error (n ) 3). Values of the left y axes show pot-basis data, and those of the right y axes show a per-hectare basis data converted from pot-basis data. Cd Balance of Soil and Rice. The Cd balance was calculated from the total soil Cd and the Cd uptake by shoots and roots of Milyang 23 (Table 2). Rates of Cd recovery after phytoextraction were more than 98% even without recovery of the leachates after watering. This result indicates that there is little possibility of losing Cd by leaching. Seed Dry Weights and Cd Concentrations of Soybeans Grown in the Three Soils. The seed DWs of the soybeans showed no significant differences between phytoextracted and control soils (see the Supporting Information, the left y axes of Figure S2). The seed DW of Enrei soybeans grown at the recommended plant density (143 000 plants ha-1) is 4.2 Mg ha-1 (29). For comparison, we converted the pot-basis seed DWs into per-hectare basis data (see the Supporting Information, the right y axis of Figure S2). These converted seed DWs were 1.0-1.4 times those of field-grown soybeans (29). These results indicate that the growth of both soybean cultivars was normal.

FIGURE 2. Cadmium concentrations of control and phytoextracted soils. **P < 0.01, *P < 0.05 (t test). Exch, exchangeable fraction; Inorg, inorganically bound fraction; Org, organically bound fraction; Oxide, oxide-occluded fraction. Entisols 1 and 2 were unlimed. Error bars show standard error (n ) 3).

TABLE 2. Mass-Balance (mg pot-1) of Cd Based on Cd Uptake by Rice and Cd Decrease in Soil

soil Cd before phytoextraction soil Cd after phytoextraction shoot Cd uptake by rice root uptake by rice total recovery rate

Andisol

Entisol 1

Entisol 2

83.7 ( 1.0

77.0 ( 1.0

77.3 ( 1.5

75.4 ( 0.9

64.9 ( 1.1

62.4 ( 1.0

6.0 ( 0.7

8.2 ( 0.5

10.4 ( 0.5

2.6 ( 0.2

3.5 ( 0.2

3.4 ( 0.1

83.9 ( 1.7 100.3%

76.6 ( 1.8 99.6%

76.3 ( 1.6 98.8%

Seed Cd concentrations were significantly lower in the phytoextracted soils in both Enrei (P < 0.01; 43% in Andisol, 41% in Entisol 1, and 29% in Entisol 2) and Suzuyutaka (P < 0.01; 24%, 46%, and 44%) (Figure 3). Relationships between Cd in Plants and Cd in Soils. Correlation analysis showed that the correlation coefficients VOL. 42, NO. 16, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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Discussion

FIGURE 3. Seed Cd concentrations of soybeans grown on control and phytoextracted soils. **P < 0.01 (t test). Error bars show standard error (n ) 3). (r) of the exchangeable fraction against the rice shoot Cd uptake and the total Cd uptake were the highest and only significant values among the seven fractions and total soil [Cd] values (see the Supporting Information, Table S1). Four simple regression equations were obtained (see the Supporting Information, Figure S3). ANOVA showed that each was significantly able to predict the shoot and total Cd uptakes by Milyang 23 from the soil [Cd] of the exchangeable and 0.01 mol L-1 HCl-extractable fractions regardless of soil type. R2 values of the exchangeable fraction were higher than those of the 0.01 mol L-1 HCl-extractable fraction. Correlation analysis showed that the r values of the exchangeable fraction and the 0.01 mol L-1 HCl-extractable fraction against the soybean seed [Cd] were the only significant positive values among the seven fractions and total soil [Cd] values (see the Supporting Information, Table S2). Four simple regression equations were obtained (see the Supporting Information, Figure S4). ANOVA showed that each was significantly able to predict the seed [Cd] of both soybean cultivars from the soil [Cd] of the exchangeable and 0.01 mol L-1 HCl-extractable fractions regardless of soil type. R2 values of the exchangeable fraction were higher than those of the 0.01 mol L-1 HCl-extractable fraction. 6170

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The order of rice shoot [Cd] was Entisol 2 > Entisol 1 > Andisol (Figure 1), the same as that of the exchangeable and 0.01 mol L-1 HCl-extractable fractions (Figure 2), but the order of the root [Cd] was not the same as that of the exchangeable fraction. Critical levels of Cd toxicity for rice are 5-10 mg kg-1 in shoots and 100-600 mg kg-1 in roots (30). The root [Cd] of the rice grown in the two Entisols was near the toxic level (90 mg kg-1). Milyang 23 translocates and accumulates more Cd in its shoots than japonica cultivars do (20), up to 36 mg kg-1 (Figure 1). The translocation and accumulation of excess Cd in shoots would be one of the mechanisms for avoiding Cd toxicity and the reason for the lack of correspondence between the root [Cd] and the exchangeable soil fractions of the two Entisols. The shoot concentrations of other metals in rice grown on the three control soils were 27.2-29.0 mg Cu kg-1, 2.5-6.5 mg Pb kg-1, and 141.6-390.4 mg Zn kg-1, and those in roots were 27.3-29.4, 7.9-19.1, and 421.1-1209.6 mg kg-1, respectively. The [Cu] and [Zn] in shoots were within or over the toxic range (20-30 and 100-300 mg kg-1, respectively), and the [Zn] in roots grown on both Entisols (747.6 and 1209.6 mg kg-1) was over the toxic range (500-1000 mg kg-1) (30). No symptoms of metal toxicity were found in any rice plant. Thus, Milyang 23 rice appears to have a high tolerance to metal toxicity, especially to Zn. The [Cd] in shoots of Milyang 23 was 19.2 mg kg-1 on Andisol and 28.0 mg kg-1 on Entisol 1 (Figure 1). These values are 2.3 and 2.5 times those in a previous study using the same soils (20). The growth period of Milyang 23 in this study was 130 days to maturity, which was 2.2 times the time to maximum tiller number stage (60 days) in the previous study. The [Cd] in rice shoots increases as the growth stage progresses from panicle formation to maturity (31). These reasons explain why the [Cd] in rice shoots in this study was higher than in the previous study. The results of correlation and regression analyses of soil Cd against plant Cd suggest that the exchangeable Cd fraction of soil is the best measure among the seven Cd fractions and the total Cd of soil for predicting the Cd uptake by Milyang 23 and the seed [Cd] of Enrei and Suzuyutaka soybeans grown on aerobic paddy soils (see the Supporting Information, Tables S1 and S2 and Figures S3 and S4). This could be an example of bioavailable contaminant stripping (32). The predicted Cd in soybean seeds does not correspond with the reported direct relation between the Cd contents in the seeds of soybeans and the soil Cd measured by extraction with 0.1 mol L-1 HCl (21). The Cd sources in our experiment were atmospheric deposition and wastewater from abandoned mines, whereas that in ref 21 was heated, anaerobically digested sewage sludge. Further, those authors used an Alfisol and used only 0.1 mol L-1 HCl extraction. Thus, there are several possible reasons for the difference between our results and those of ref 21. Milyang 23 accumulated 7-14% of the total soil Cd in its shoots (Table 1, Figure 1) and decreased several Cd fractions by 8-42% and the total soil Cd by 10-19% (Figure 2). Indian mustard (Brassica juncea (L.)) and the hyperaccumulator Thlaspi caerulescens accumulated 0.09% and 0.06% of the total soil Cd (40 mg kg-1) when grown for 6 weeks in pots (9). Nicotiana rustica L. accumulated 6% and N. tabacum L. accumulated 20% of the total soil Cd (5.44 mg kg-1) when grown for 8 weeks in containers (14). Thus, Milyang 23 has the potential to phytoextract soil Cd with a similar efficiency as those Nicotiana species. The seed [Cd] of the soybeans grown on the phytoextracted soils was 24-44% lower than that in the control soils (Figure 3). These rates of reduction are higher than those of soil washing (about 25%) with CaCl2 (33). Soil washing is generally

not environmentally sound and costs more than phytoextraction (6, 34). Washing with CaCl2 decreases only the exchangeable and acid-soluble (inorganically bound) Cd fractions (35), whereas Milyang 23 decreased the organically bound Cd fraction as well (Figure 2). Soybean culture decreased these three soil Cd fractions also (20). These results suggest that phytoextraction by Milyang 23 has the potential to reduce the [Cd] of soybean seeds more efficiently than can soil washing with CaCl2. The seed [Cd] of soybeans was still high even after phytoextraction by Milyang 23. The maximum level for Cd in soybean seeds (15% water content) proposed by Japan is 0.5 mg kg-1 (36). It would need at least 1.4 times the phytoextraction in the field to obtain the same results as in this pot experiment (as stated in the Results). If we suppose that 0.59 mg kg-1 is the dry-based maximum permissible value for Cd in soybean seeds, and phytoextraction by rice in pots is consistently 1.4 times as effective at reducing soybean seed [Cd] as in the field, it would take three phytoextractions on Andisol, five on Entisol 1, and nine on Entisol 2 to reduce seed [Cd] to the maximum permissible level in Enrei soybean, and seven, five, and six in Suzuyutaka. This implies that phytoextraction by Milyang 23 is economically feasible. The soybean seed [Cu] on all soils ranged from 5.5 to 11.6 mg kg-1, and the seed [Zn] on Andisol and Entisol 2 ranged from 33.7 to 59.4 mg kg-1. These values are below or within the range of normal values in soybeans in Japan (10.0-21.5 mg Cu kg-1 and 36.0-68.0 mg Zn kg-1) (37). Pb was not detected in seeds. The seed [Zn] on Entisol 1 (70.5-86.4 mg kg-1) was above the normal range but less than excessive (114 mg kg-1) (38). The seed [Zn] on phytoextracted Entisol 1 decreased by 18.4% from that on control soil to 70.5 mg kg-1 in Enrei, and by 7.1% to 73.8 mg kg-1 in Suzuyutaka. Five phytoextractions of Entisol 1 to reduce seed [Cd] to the maximum permissible level would be sufficient to reduce seed [Zn] to the normal level. Judging from these results, we conclude that phytoextraction by Milyang 23 rice is a promising remediation method for reducing the seed [Cd] of soybeans grown on aerobic paddy soils contaminated with moderate [Cd]. Field experiments are now in progress on several paddy fields in Japan.

Acknowledgments We thank Ms. M. Tozawa, Ms. A. Onuki, Mr. N. Imai, and Mr. M. Setagawa for their help in the greenhouse and the laboratory at NIAES. This work was supported by a Grantin-Aid (Hazardous Chemicals) from the Ministry of Agriculture, Forestry and Fisheries of Japan (HC-05-1160).

Supporting Information Available Soil and plant analyses and additional figures and tables. This information is available free of charge via the Internet at http://pubs.acs.org.

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