Growth inhibition of rice (Oryza sativa L.) seedlings in Ga- and In-contaminated acidic soils is respectively caused by Al and Al + In toxicity

Journal of Hazardous Materials 344 (2018) 274–282

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Research Paper

Growth inhibition of rice (Oryza sativa L.) seedlings in Ga- and In-contaminated acidic soils is respectively caused by Al and Al + In toxicity Jeng-Yan Su a,1 , Chien-Hui Syu b,1 , Dar-Yuan Lee a,∗ a b

Department of Agricultural Chemistry, National Taiwan University, No. 1, Sec. 4, Roosevelt Rd., Taipei 10617, Taiwan Division of Agricultural Chemistry, Taiwan Agricultural Research Institute, No.189, Zhongzheng Rd., Wufeng Dist., Taichung City 41362, Taiwan

g r a p h i c a l

a b s t r a c t

h i g h l i g h t s • Growth inhibition of rice plant in Ga-spiked acidic soils is due to Al toxicity. • Growth inhibition of rice plant in In-spiked acidic soils is due to Al + In toxicity. • Growth inhibition of rice plant by Ga and In in neutral/alkaline soils is negligible.

a r t i c l e

i n f o

Article history: Received 23 June 2017 Received in revised form 6 October 2017 Accepted 10 October 2017 Available online 12 October 2017 Keywords: Emerging contaminants Gallium

a b s t r a c t Limited information exists on the effects of emerging contaminants gallium (Ga) and indium (In) on rice plant growth. This study investigated the effects on growth and uptake of Ga and In by rice plants grown in soils with different properties. Pot experiment was conducted and the rice seedlings were grown in two soils of different pH (Pc and Cf) spiked with various Ga and In concentrations. The results showed concentrations of Ga, In, and Al in soil pore water increased with Ga- or In-spiking in acidic Pc soils, significantly decreasing growth indices. According to the dose-response curve, we observed that the EC50 value for Ga and In treatments were 271 and 390 mg kg−1 in Pc soils, respectively. The context of previous hydroponic studies suggests that growth inhibition of rice seedlings in Ga-spiked Pc soils is

∗ Corresponding author. E-mail address: [email protected] (D.-Y. Lee). 1 Mr. Jeng-Yan Su and Dr. Chien-Hui Syu are equal contributors to this paper. https://doi.org/10.1016/j.jhazmat.2017.10.023 0304-3894/© 2017 Elsevier B.V. All rights reserved.

J.-Y. Su et al. / Journal of Hazardous Materials 344 (2018) 274–282 Indium Aluminum Rice seedlings

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mainly due to Al toxicity resulting from enhanced Al release through competitive adsorption of Ga, rather than from Ga toxicity. In-spiked Pc soils, both In and Al toxicity resulted in growth inhibition, while no such effect was found in Cf soils due to the low availability of Ga, In and Al under neutral pH conditions. © 2017 Elsevier B.V. All rights reserved.

1. Introduction Gallium (Ga) and indium (In) compounds are being extensively utilized in semiconductor manufacturing and the electro-optical industry [1,2]. The present vigorous development of high-tech industries raises the concern that large amounts of wastewater derived from associated manufacturing processes may easily become a potential source of environmental contamination. Once industrial effluents containing Ga and In are discharged into rivers or through irrigating systems, their presence may influence the growth and productivity of crops. Humans may also be exposed to Ga and In via the food chain, which could pose severe health risks. Studies have suggested that Ga and In metalloids are generally toxic to laboratory animals and may potentially cause testicular toxicity and increase tumor occurrence [3]. Chepesiuk [4] also found that exposure to gallium arsenide (GaAs) and indium arsenide (InAs) can result in both acute and chronic toxicity to the lungs, kidneys, and reproductive organs. Considering that groundwater concentrations of Ga and In in science-focused industrial parks are significantly higher than those of non-industrial areas in Taiwan [5], a wider understanding is needed to further assess the potential impact of Ga and In-containing wastewater on the environment. Ga and In are amphoteric elements placed in the IIIA group in the periodic table. Their species depend on the pH and oxidation state of the environment. The valence of both elements is generally + 3, while oxidation states of + 1 or + 2 can also exist dependent on environmental conditions [1]. At room temperature, soluble species such as Ga3+ , Ga(OH)2 + , Ga(OH)2+ , In3+ , In(OH)2 + , and In(OH)2+ are predominant under acidic conditions, while In can be transformed into the insoluble In(OH)3 at pH 5–9 [1,6]. The chemical characteristics of Ga and In are similar to those of Aluminum (Al), and several studies have reported on Al dynamics in soils and on related toxicity to rice plants [7–9]. However, little information about the effects of Ga and In on the growth of rice plants grown in Ga/In-contaminated soils exists to date. Rice (Oryza sativa L.) is the staple food for over 90% of the population in Asia [10]. This universal food item may represent a potential route by which human beings are exposed to Ga and In, especially in areas near high-tech industrial parks. Our previous study showed that exposing rice seedlings to Ga and In in hydroponic experiments had different effects on the growth of rice plants. A significant increase in growth indices was observed with increasing Ga concentration in culture solutions (<10 mg Ga L−1 ), which suggests that Ga may accelerate the growth of rice seedlings. In contrast, under In exposure, nutrient deficiency and growth inhibition occurred when In concentrations were higher than 0.04 mg L−1 [11]; the toxicity mechanism was similar to that of Al toxicity [12]. In addition, Kopittke et al. [13] also found that adding soluble Ga and In to cowpeas in solution culture caused cell rupture within 2 h and reduced the elongation of cowpea roots. Yu et al. [14] found that Ga retarded the relative growth rate, transpiration rate, and water-use efficiency of rice seedlings after 2 days of exposure to increasing Ga concentrations in solution culture. Due to the complexity of paddy soils, factors like pH, redox potential, cation exchange capacity (CEC), and organic matter content all affect the fate of Ga and In in soils. Consequently, the effects of Ga and In on rice seedlings in hydroponic experiments might differ from those in soil cultiva-

tion. Existing literature on the dynamics of Ga and In elements in various soil systems is relatively scarce. Therefore, the objective of this study was to investigate the effects of Ga and In on the growth of rice seedlings and to assess the fate of these elements in various soil systems. 2. Materials and methods 2.1. Soil sampling and properties Surface soils (0–30 cm) were randomly collected from the Pinchen series, Taoyuan (northern Taiwan), and the Chengchung series, Tainan (southern Taiwan). Soil samples were air-dried, sieved to a particle size below 2 mm, homogenized, and preserved in plastic vessels. Basic properties were determined as follows. Soil pH was measured at a 1:1 ratio of soil to water [15]. The hydrometer method [16] was used to determine soil texture. Cation exchange capacity (CEC) was determined using the NH4 OAC method [17]. Organic matter content was determined by the Walkley–Black wet digestion method [18]. Crystalline and amorphous iron and aluminum contents were extracted with dithionite-citrate-bicarbonate (DCB) and ammonium oxalate, respectively [19,20]. Plant available-aluminum (Al) in soils was determined by the 0.02 M calcium chloride (CaCl2 ) extraction method [21]. The basic physical and chemical properties of the two tested soils are presented in Table 1. The Pinchen soil (Pc) had low pH, CEC, and O.M, which are notable features of acidic soils (pH = 4.1). In contrast, the Cf soil had high pH (pH = 7.4) and CEC. The textures of the Pc and Cf soils were clay and silty clay loam, respectively. Both amorphous Al content and Fe oxide were lower in Cf soils than in Pc soils. Native Ga concentrations in Pc and Cf were 22 and 11 mg kg−1 , respectively; In concentrations were below the detection limit. 2.2. Ga and In treatment The two tested soils were prepared by artificially spiking with GaCl3 (99.999%, ultra dry; Alfa Aesar) and InCl3 (99.999%, anhydrous; Alfa Aesar), respectively. Concentrations of both treatments were 0, 50, 100, 200, and 400 mg kg−1 . Each treatment was prepared in three replicates. 2.3. Pot experiments The Taikeng 9 cultivar of paddy rice (Oryza sativa L.) was used in this study due to its high quality and because it is commonly planted in Taiwan. Rice seeds were sterilized by soaking in a solution containing 30% hydrogen peroxide and 1% sodium hydrochloride for 30 min, then rinsed with distilled water several times to make sure the residual solution was completely washed away. For pregermination, seeds were placed on moist tissue paper in Petri dishes at 37 ◦ C for 4 days. After germination, rice seedlings were transferred into unspiked soils and grown for 14 days. Four wellgrown seedlings were selected and transplanted together into each one pot filled with 500 g of the Ga or In-spiked soils for 50 days of cultivation. Each treatment was conducted in three replicates. Water levels of pots were maintained at about 5 cm above the soil

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Table 1 The basic properties of studied soils. pH

Pc Cf

4.1 7.4

Texture

Ca SCLa

CEC

O.M.

cmol kg−1

g kg−1

7.8 9.3

9 15

Feo

Alo

Fed

Ald

Gatotal

Intotal

mg kg−1 2.9 3.1

2 0.8

32.9 7.9

6.2 1.5

22 8

7 3

O.M.: Organic matter. Feo , Alo : ammonium oxalate extractable Fe and Al. Fed , Ald : dithionite–citrate–bicarbonate (DCB) extractable Fe and Al. a C: Clay, SCL: Silty clay loam.

surface throughout the whole cultivation period. Soils were supplemented with 58.98 mg urea [CO(NH2 )2 ], 44.4 mg monocalcium phosphate [Ca(H2 PO4 )2 H2 O], and 71.25 mg potassium chloride (KCl) for each pot as basal fertilizers. Pot experiments were carried out in the phytotron of National Taiwan University at a controlled temperature (20/25 ◦ C, night/day) and relative humidity (70–95%) under natural sunlight throughout the cultivation period. The pH and redox potential (Eh) of soils during the cultivation period were regularly monitored with portable meters. After harvesting, rice seedlings were rinsed with tap water and divided into roots and shoots with ceramic scissors, and root biomass and shoot biomass and height were measured.

2.4. Soil pore water sampling Soil pore water was collected using rhizon samplers (10 Rhizon SMS, Rhizosphere research products). Samplers connected to syringes were inserted into soils near the middle of each pot at an angle of 45◦ to extract soil pore water during the cultivation period. The collected solution was filtered through a 0.45-␮m filter. To prevent Ga and In from precipitating, the filtrate was preserved in 5% nitric acid (HNO3 ) immediately after filtration. A portion of the solution was diluted with deionized water to determine the Ga and In concentration in soil pore water as an index representing the availability of in these elements in the soils. The Al concentration in soil pore water was also determined. Determination of Ga and In concentrations was carried out by inductively coupled plasma mass spectroscopy (ICP-MS 7700x; Agilent Technologies), and the concentration of Al was determined by inductively coupled plasma-optical emission spectrometry (ICP-OES, Optima 2000 DV; PerkinElmer). All experiments were conducted in three replicates.

Table 2 The shoot height, root biomass and shoot biomass of rice seedlings grown in two tested soils with different Ga and In treatments.

Treatments

Shoot height cm

Root biomass g plant−1

Shoot biomass g plant−1

Pc-Ga PcCK PcGa50 PcGa100 PcGa200 PcGa400

51.2 ± 0.2a * 51.5 ± 0.4 a 45.6 ± 0.4 b 28.3 ± 2.9 c 19.9 ± 0.3 d

0.28 ± 0.01 a 0.20 ± 0.06 b 0.09 ± 0.01 c 0.04 ± 0.00 d 0.03 ± 0.00 d

0.64 ± 0.01 a 0.43 ± 0.01 b 0.24 ± 0.02 c 0.10 ± 0.02 d 0.08 ± 0.01 d

Cf-Ga CfCK CfGa50 CfGa100 CfGa200 CfGa400

40.3 ± 1.3 a 40.5 ± 1.0 a 39.8 ± 2.3 a 41.6 ± 1.6 a 42.2 ± 0.9 a

0.23 ± 0.02 ab 0.22 ± 0.05 b 0.25 ± 0.02 ab 0.25 ± 0.02 ab 0.28 ± 0.00 a

0.42 ± 0.01 a 0.44 ± 0.07 a 0.43 ± 0.04 a 0.45 ± 0.03 a 0.47 ± 0.02 a

Pc-In PcCK PcIn50 PcIn100 PcIn200 PcIn400

51.2 ± 0.2 b 52.9 ± 0.5 a 52.1 ± 0.1 ab 47.3 ± 0.8 c 22.4 ± 0.7 d

0.28 ± 0.01 a 0.30 ± 0.01 a 0.18 ± 0.04 b 0.07 ± 0.01 c 0.04 ± 0.01 c

0.64 ± 0.01 b 0.75 ± 0.00 a 0.56 ± 0.08 c 0.22 ± 0.03 d 0.09 ± 0.0 e

Cf-In CfCK CIn50 CfIn100 CfIn200 CfIn400

40.3 ± 1.3 a 39.7 ± 1.8 a 40.9 ± 3.8 a 40.0 ± 1.4 a 43.0 ± 0.3 a

0.23 ± 0.02 ab 0.18 ± 0.01 b 0.18 ± 0.03 b 0.19 ± 0.02 b 0.26 ± 0.04 a

0.42 ± 0.01 ab 0.40 ± 0.04 b 0.40 ± 0.01 b 0.43 ± 0.01 ab 0.46 ± 0.06 a

* Different letters indicated the differences in the value among the Ga/In treatments based on the LSD test.

3. Results 3.1. The growth of rice seedlings as affected by Ga and In treatments

2.5. Plant digestion and analysis Plant tissue samples of rice seedlings were oven-dried at 70 ◦ C and ground into fine powder for acid digestion. Dried plant samples (0.1–0.2 g) were digested in concentrated HNO3 /H2 O2 in heating blocks [22]. The final solution was diluted to 50 mL with deionized water, filtered, and stored in plastic bottles at 4 ◦ C until analysis. Each treatment was conducted in three replicates. The concentration of Ga and In in the digests was determined by ICP-MS, and that of Al by ICP-OES.

2.6. Data analysis Data presented in this study are means (n = 3) ± standard deviation (SD). Statistical analysis was carried out by analysis of variance (ANOVA) to test the effects of the Ga and In treatments on rice plant growth (biomass and shoot height) in different soil systems. To test for differences among the treatments, we used the least significant difference (LSD) test at a significance level of P = 0.05. Both ANOVA and LSD tests were performed using the SAS 9.2 software package.

Table 2 shows the root biomass, shoot biomass, and shoot height of rice seedlings grown in the two tested soils under different Ga and In treatments. For Pc soils, One-Way ANOVA analysis indicated that there were significant differences in the shoot height (Ga treatments: P < 0.001; In treatments: P < 0.001), root biomass (Ga treatments: P < 0.001; In treatments: P < 0.001), and shoot biomass (Ga treatments: P < 0.001; In treatments: P < 0.001) of rice seedlings among the Ga and In treatments. However, there were no significant differences in shoot height, root biomass, or shoot biomass of rice seedlings grown in Cf soils (P > 0.05), with the exception of root biomass under In treatments (P < 0.05). For Pc soils, growth indices were all decreased with Ga concentrations in soils, and the extent of the decreases of these growth indices were 11–61%, 28–87%, and 33–88% for shoot height, root biomass, and shoot biomass of rice seedlings, respectively. In contrast, for Cf soils there was no significant correlation between either Ga or In concentration and growth indices. Similarly, for In treatments, the growth indices all also decreased with In concentrations in soils, and the extent of the decreases were 7–56%, 19–82%, and 12–85% for the shoot height, root biomass, and shoot biomass of rice seedlings grown in Pc soils,

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Fig. 1. The Ga and In concentrations in pore water of Pc and Cf soils with different (a-b) Ga and (c-d) In treatments during the growth period. (The spike of 0, 50, 100, 200 and 400 mg kg−1 Ga/In in tested soils are expressed as CK, Ga/In50, Ga/In100, Ga/In200 and Ga/In400).

respectively, but there were no uniform trends in Cf soils. These differences in extent of growth inhibition depending on soil type were found to result from differences in concentrations of Ga/In/Al in soil pore water and consequently in the rice seedlings grown in the tested soils, as described below.

3.2. Concentrations of Ga, In and Al in soil pore water and CaCl2 -extractable Al of soils as affected by Ga and In treatments The concentrations of Ga and In in the pore water of the two tested soils are shown in Fig. 1. For both Ga and In treatments, element concentrations in pore water increased with spiked concentration in the two tested soils. Pore water Ga decreased with growth time in all Ga treatments. The extent of this decrease was higher in Cf soils than in Pc soils when the concentration of Ga in soils was above 200 mg kg−1 . In addition, the Ga concentration in pore water from Pc soils was higher than in Cf soils for the same Ga-spiked treatments (Fig. 1a, b). For In treatments, concentration of In in the pore water of Pc soils decreased with growth time in all treatments, but such changes were not obvious in any Cf soil treatments. In addition, In concentration in pore water from Pc soils was much higher than in Cf soils for the same In-spiked treatments. The maximum In concentration levels in pore water on the 50th day of growth time in the In400 treatments were 202 ␮g L−1 for Pc soils and 0.75 ␮g L−1 for Cf soils (Fig. 1c, d). Fig. 2 shows the concentration of Al in pore water from Pc soils under different Ga and In treatments. Concentration of Al increased with Ga- and In-spiked concentrations in Pc soils. These concentrations gradually decreased with time under the Ga treatments (Fig. 2a), and there were no obvious changes under In treatments during the growth period (Fig. 2b). Al concentrations in pore water from Pc soils with Ga treatments were higher than in In treatments with the same amount of spiking. For instance, on the 50th day

Table 3 The concentrations of CaCl2 extractable-Al in two tested soils with different Ga and In treatments.

Treatments

CaCl2 extractable-Al mg kg−1

Treatments

CaCl2 extractable −Al mg kg−1

Pc soil PcCK PcGa50 PcGa100 PcGa200 PcGa400

50.82 ± 0.1 e, * 74.94 ± 027 d 81.60 ± 0.48 c 94.76 ± 1.25 b 132.8 ± 0.20 a

PcCK PcIn50 PcIn100 PcIn200 PcIn400

50.82 ± 0.1 e 70.56 ± 0.56 d 74.93 ± 0.45 c 80.86 ± 0.06 b 96.72 ± 0.51 a

Cf soil CfCK CfGa50 CfGa100 CfGa200 CfGa400

n.d. n.d. n.d. n.d. n.d.

CfCK CIn50 CfIn100 CfIn200 CfIn400

n.d. n.d. n.d. n.d. n.d.

n.d.: not detection. * Different letters indicated the differences in the value among the Ga/In treatments based on the LSD test.

of growth, Al concentrations in PcGa400 and PcIn400 were 32 and 15 mg L−1 , respectively (Fig. 2a, b). In addition, there was a significant positive correlation between the Ga/In concentration in Pc soils and the average Al concentration in soil pore water (Ga treatments: R2 = 0.9530, P < 0.01; In treatments: R2 = 0.9645, P < 0.01) (Fig. 2c). However, Al concentration levels in pore water from Cf soils were below the detection limit of ICP-MS for all treatments (data not shown). In addition, Table 3 shows the concentration of CaCl2 -extractable Al in soils. This can be used as an index showing that plant-available Al increased with Ga and In concentration in Pc soils. It also shows that the concentration of CaCl2 -extractable Al from Pc soils with Ga treatments was higher than under identical In treatments; however, in Cf soils it was always below the detection limit.

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soils (roots: 0.5–201.1 mg kg−1 ; shoots: 0–8.3 mg kg−1 ) was much higher than in those grown in Cf soils (roots: 0.2–55.8 mg kg−1 ; shoots: 0–1.3 mg kg−1 )(Fig. 3e–h). Apparently it was also difficult for In to be translocated from the roots to the shoots, especially in Cf soils under high In treatments (soil In > 200 mg kg−1 ), supporting the finding of In concentration in roots being 28–42 folds higher than in shoots (Fig. 3g, h). Fig. 4 shows Al concentration in roots and shoots of rice seedlings grown in two soils under Ga and In treatments. For Ga treatments, the concentration of Al in the roots and shoots increased with increased Ga concentration in Pc soils, and there was a significant increase in Al concentration in those tissues when the Ga concentration in soils was higher than 200 mg kg−1 (Fig. 4a, b). In contrast, no uniform trends in Al concentration could be found in In treatments in Pc soils (Fig. 4e, f). Al concentrations in roots in Pc soils were about one order of magnitude higher than in shoots, similar to the pattern for Ga and In noted above (Fig. 3), but such trends were absent in Cf soils (Fig. 4c–d, g–h). Al concentrations in roots were 2–4 folds higher than in shoots. Overall, seedlings grown in Pc soils had higher Al concentrations than those grown in Cf soils at the same levels of Ga/In treatment. There was no significant negative correlation between Al and Ga/In concentration in roots or shoots (data not shown).

4. Discussion

Fig. 2. The Al concentrations in soil pore water of Pc soil with different (a) Ga and (b) In treatments during the growth period, and (c) the correlation between the Ga/In concentrations in Pc soils and the average Al concentrations in pore water. (The spike of 0, 50, 100, 200 and 400 mg kg−1 Ga/In in tested soils are expressed as CK, Ga/In50, Ga/In100, Ga/In200 and Ga/In400).

3.3. Concentrations of Ga, In, and Al in rice seedlings as affected by Ga and In treatments Concentrations of Ga or In accumulated in the roots and shoots of rice seedlings are shown in Fig. 3. For Ga treatments, the concentration of Ga in roots and shoots increased with the concentration of Ga-spiked in both soils. Concentrations in plant tissues in Pc soils was not significantly increased when the Ga concentrations over 100 mg kg−1 in soils. Concentrations of Ga in roots (5–127 mg kg−1 ) and shoots (3.6–10 mg kg−1 ) in Pc soils was higher than in Cf soils (roots: 5–114 mg kg−1 ; shoots: 0.6–7.5 mg kg−1 ) under the same level of Ga treatment (Fig. 3a–d). Ga concentration in roots was about one order of magnitude higher than in shoots under most of the Ga treatments in both soils (Pc: 1.3–12.6 folds; Cf: 9.0–25.6 folds). For In treatments, In concentration in roots and shoots also increased with the concentration of In-spiked in both soils (Fig. 3e–g), except for the In accumulated in shoots in Cf soils (Fig. 3h). The concentration of In in plant tissues grown in Pc

In our experiment, growth indices clearly showed that shoot height and biomass of roots and shoots of rice seedlings significantly decreased with Ga concentration in Pc soils, but that there were no significant differences in those growth indices among Ga treatments in Cf soils (Table 2). In our previous hydroponic study, the growth of rice seedlings of a similar cultivar was not inhibited but enhanced in a culture solution containing 0–15 mg L−1 Ga [11]. In the present study, the average concentrations across the growth period of Ga in pore water from Pc and Cf soils under Ga400 treatment were 411 and 122 ␮g L−1 , respectively (Fig. 1a, b); both measures are much lower than the toxicity threshold of Ga to rice plants. This suggests that despite increased Ga concentration in pore water, the inhibition of rice plant growth in Ga-spiked Pc soils did not directly result from Ga toxicity (Fig. 1). Due to the high activity of soluble Al species (Al3+ ) in acidic soils [7], it is however possible that Al could be released into soil pore water via the addition of Ga and In to Pc soils (Fig. 2). By contrast, the formation of insoluble Al species (Al(OH)3 ) in neutral soils [23] resulted in concentration levels of Al in the pore water of Cf soils that were below the detection limit (and resulted in no growth inhibition). This suggests that the phytotoxicity of rice seedlings in Pc soils might be caused by Al toxicity under Ga treatments. Al concentration in pore water and CaCl2 extracts (plant-available form) were both also found to increase with the addition of Ga and In (Fig. 2, Table 3), and there was a significant positive correlation between the concentration of pore water-Al and plant-available Al (R2 = 0.8691, P < 0.001; data not shown), which mainly resulted from competitive adsorption between Ga/In and Al on the soil surface. Foy [24] reported that Al toxicity is the dominant growth-limiting factor for plants in acidic soils. Bidhan and Sanjib [25] noted that the shoot height and seedling fresh weight of some rice genotypes were significantly decreased grown in a nutrient solution containing 30 mg Al L−1 . In the present study, shoot height and seedling biomass were significantly reduced when the Al concentration in soil pore water was above 5 mg L−1 (Fig. 2a). Similarly, the finding that in Pc soils the concentration of Al in pore water also increased with In concentration (Fig. 2b) suggests that Al toxicity might be one of the causes for the growth inhibition of rice seedlings in In-spiked Pc soils. However, no significant

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Fig. 3. The concentrations of (a–d) Ga and (e–h) In in roots and shoots of rice seedlings grown in Pc and Cf soils with different Ga treatment. (The spike of 0, 50, 100, 200 and 400 mg kg−1 Ga/In in tested soils are expressed as CK, Ga/In50, Ga/In100, Ga/In200 and Ga/In400).

differences in growth indices were found between the PcGa400 and PcIn400 treatments (Table 1), and the concentration of Al in soil pore water under PcIn400 treatments was lower than under PcGa400 treatments (Fig. 2c). In addition, In concentration in soil pore water under PcIn400 treatments was higher than 0.08 mg L−1 in this study (Fig. 1c), a concentration level that was found to inhibit

growth and nutrient uptake in this rice cultivar in our previous hydroponic study [11]. This suggests that the phytotoxicity of rice seedlings in In-spiked soils might be caused not only by Al toxicity but also by In toxicity under the PcIn400 treatment. These results thus suggest that Al toxicity was the dominant factor causing the growth inhibition of rice seedlings when the In concentration in Pc

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Fig. 4. The concentrations of Al in roots and shoots of rice seedlings grown in Pc and Cf soils with different (a-d) Ga and (e–h) In treatments. (The spike of 0, 50, 100, 200 and 400 mg kg−1 Ga/In in tested soils are expressed as CK, Ga/In50, Ga/In100, Ga/In200 and Ga/In400).

soils was lower than 200 mg kg−1 , and that the growth inhibition of rice seedlings in 200 and 400 mg In kg−1 Pc soils was caused by both Al and In toxicity. However, for Cf soils, insoluble In(OH)3 00 was the predominant species under neutral pH [6]; this had no significant effect on growth (Table 1). In addition, according to the correlation between the Ga/In concentration in Pc soils and the average Al concentration in pore water (Fig. 2c), the slope of the Ga treatment was higher than that for the In treatment. This suggests that Al was

more easily replaced by Ga than by In, which agrees with the fact that the atomic radius of Ga (0.135 nm) is closer to Al (0.143 nm) than In (167 nm). Burton and Culkin [26] have also suggested that due the similarity in ionic radii between Ga and Al, Al3+ could be replaced by Ga3+ in soil (rock)-forming processes. Except for the above reasons, the organic matter in soils may also affect the toxicity of Ga, In and Al on the growth of rice seedlings, due to that it is recognized as a complexing agent for metals, which could affect

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the dynamics of these metals in soils [27,28]. In this study, it was found that the amounts of organic matter in Cf soils were higher than those in Pc soils (Table 1), which may reduce the bioavailability and phytotoxicity of Ga, In, and Al in Cf soils through the sorption (complexation and adsorption) reactions (Fig. 1, Table 2). Moreover, it was also observed that the Ga concentration in pore water in Cf soils of various Ga treatments increased at 15th day of growth period (Fig. 1b), which might be resulted from the degradation of a portion of organic matter during plant growth, thus releasing Ga from its complexes and the surface adsorption sites. Therefore, it suggests that the extent of phytotoxicity of Ga and In to rice plants in Ga- and In-contaminated soils is not only controlled by soil pH, but also by the contents and decomposability of organic matter. Plant tissue analysis showed that the concentrations of all three elements in roots were about one order of magnitude higher than in shoots (Fig. 3). This suggests that roots are a major sink of Ga, In, and Al accumulation in rice plants, which is consistent with the findings of earlier hydroponic studies [11,14,29]. However, there exists limited information about Ga and In uptake and distribution in different parts of plants grown in soil systems. Al toxicity might also result in low accumulation of Ga in rice tissues, which would accord with the finding that Ga concentrations in roots and shoots reached a plateau under high-Ga treatments (>100 mg Ga kg−1 ) in Pc soils, and that In concentration in shoots decreased at soil In concentrations above 200 mg kg−1 . Although in Cf soils Ga concentrations in seedlings were not affected by Al toxicity, the accumulation of In in shoots was slightly affected by In toxicity under high-In treatments (>200 mg In kg−1 ) (Fig. 3). The Al concentration in seedlings was 100-fold higher than that for Ga/In, which may have resulted from that fact that the concentration of Al in pore water was much higher than for Ga/In. In addition, there was no significant negative correlation between Al and Ga/In concentration in roots and shoots. These results indicate that there was no obvious antagonism (competitive absorption) between Al and Ga/In in rice seedlings. The physiological mechanisms resulting in the different Ga and In accumulation in rice plants under various Ga/In concentration levels in soil remain unclear and require further investigation.

5. Conclusions In summary, the results of this study indicate that the dynamics of Ga and In and their phytotoxicity to rice seedlings are affected by soil characteristics. For both Ga and In, the solubility and concentration in soil pore water in acidic soils (Pc soils) were higher than in neutral soils (Cf soils), due to differences in Ga and In species present under different pH conditions. For the acidic soils with their high concentration of available Al (Pc soils), the release of Al increased with increasing Ga- and In-spiked concentration in soils, leading to Al phytotoxicity and inhibited growth of rice seedlings. The phytotoxic response of rice plants to In also occurred in the high-In-contaminated soils (>200 mg In kg−1 in Pc soils). The EC50 (effective concentration resulting in 50% growth inhibition) values for the Ga and In treatments in Pc soils were 271 and 390 mg kg−1 , respectively, based on the dose-response curve as shown in Fig. 5. In contrast, for pH-neutral soils (low-Al Cf soils) the growth of rice seedlings was not inhibited by any Ga and In treatments. We therefore suggest that for rice plants grown in acidic Ga- and Incontaminated soils, phytotoxicity induced by not only Ga and In but also Al should be a source of concern, while these effects are negligible in neutral soils. In addition to the phytotoxic effects, further investigation of the accumulation of Ga and In in rice grains grown in contaminated soils is required to assess any health effects on humans.

281

Fig. 5. Dose-response relation model as a function of the concentration of Ga/In in soils for the relative shoot height of rice seedlings grown in Pc soils under Ga/In treatments.

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