JXB Advance Access originally published online on July 2, 2004
Journal of Experimental Botany 2004 55(403):1707-1713; doi:10.1093/jxb/erh205
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RESEARCH PAPER |
Do iron plaque and genotypes affect arsenate uptake and translocation by rice seedlings (Oryza sativa L.) grown in solution culture?
1Research Center for Eco-environmental Sciences, Chinese Academy of Sciences, China
2College of Natural Resources and Environment, Hebei Agricultural University, Baoding, Hebei Province, China
3Soil and Land Systems, School of Environmental Sciences, The University of Adelaide, Adelaide, South Australia 5005, Australia
* To whom correspondence should be addressed. Fax: +86 10 6292 3563. E-mail: ygzhu{at}mail.rcees.ac.cn
Received 30 December 2003; Accepted 13 May 2004
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Abstract |
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The effects of Fe concentrations in the pretreatment solution on the induction of plaque and the differences between genotypes on arsenate uptake by and translocation within rice seedlings grown in nutrient solution in the greenhouse were investigated. After iron plaque on rice roots was induced in solutions containing 20, 40, 60, 80, and 100 mg Fe2+ l–1, seedlings were transplanted into nutrient solution with 0.5 mg As l–1. The formation of iron plaque was clearly visible as a reddish coating on the root surface after 12 h induction. Fe2+ concentrations in the pretreatment solution and 0.5 mg As l–1 in the treatment solutions did not significantly affect rice growth. There was a significant correlation between the concentrations of Fe and As in iron plaque on the root surface for the three genotypes. About 75–89% of total As was concentrated in iron plaque (DCB-extracts). There were no significant differences in As concentrations in the roots between the three genotypes; however, As concentrations in shoots differed significantly between them. Arsenic concentrations in shoots were positively correlated with iron concentrations in the shoots. The results suggest that iron plaque may act as a ‘buffer’ for As in the rhizosphere.
Key words: Arsenic translocation, arsenic uptake, iron plaque, rice genotypes
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
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Arsenic (As) is a ubiquitous metalloid, widely distributed in the environment through both natural and anthropogenic pathways. Background levels of As in soils are 5–6 mg kg–1 dry soil on average (Yan, 1994
). However, anthropogenic activities, such as pesticide and herbicide application (Maclean and Langille, 1981), mining (Galbraith et al., 1995), or irrigation with contaminated groundwater (Abedin et al., 2002a, b), have significantly enhanced As levels in the soil environment (Marin et al., 1992). Geogenic As-contaminated groundwater has been reported in many countries, especially in Bangladesh (Dhar et al., 1997; Biswas et al., 1998; Nickson et al., 1998; Chowdhury et al., 1999, 2000), West Bengal, and India (Mandal et al., 1996). The people of these regions not only drink the contaminated groundwater, but also irrigate crops with it. Therefore, the transfer of As in soil–plant systems represents one of the principal pathways for human exposure to As (Juhasz et al., 2003).
Rice (Oryza sativa) is the staple food for people in many parts of the world, particularly South-East Asia. In Bangladesh, irrigation is mostly dependent on groundwater, and 75% of the total cropped area and 83% of the total irrigated area are irrigated using groundwater for rice cultivation (Dey et al., 1996; Abedin et al., 2002a). It has been reported that As levels in the soils of these areas could reach over 80 mg kg–1 after continuous irrigation with contaminated water (Ullah, 1998; Abedin et al., 2002a). Under irrigation with As-contaminated groundwater, rice straw, which is fed to cattle in Bangladesh and India, can also accumulate high levels (up to 92 mg kg–1) of As (Abedin et al., 2002b). Some studies suggested that As can easily be accumulated in roots and translocated to rice shoots. Moreover, rice grown on As-contaminated paddy soils can also accumulate high levels of As in grains (Xie and Huang, 1998). Thus As uptake by rice plants plays an important role in the transfer of this toxic element into food chains and poses health risks to human beings (Meharg and Rahman, 2003).
Iron plaque is commonly formed on the roots of aquatic plant species, such as Oryza sativa, Typha latifolia L., and Phragmites australis Trin. The iron plaque may be amorphous or crystalline (Bacha and Hossner, 1977; Chen et al., 1980). It is composed mainly of ferrihydrite (63%) with lesser amounts of goethite (32%) and minor levels of siderite (5%) (Hansel et al., 2001). Some reports have shown that iron plaque may be a barrier to the uptake of heavy metals, such as Cu, Ni, Mn, and Cd (Taylor and Crowder, 1983a; Otte et al., 1989; Greipsson, 1994; Ye et al., 1998; Wang and Peverly, 1999). However, the overall effect of iron plaque on plant uptake of nutrients and/or contaminants may depend on the amount of iron plaque that is formed on the plant roots (Otte et al., 1989; Zhang et al., 1998). The functional groups of iron hydroxides may sequestrate some cations and anions (Kuo, 1986; Otte et al., 1989). Meng et al. (2002) found that iron hydroxides in soil or solution had a very strong binding affinity for arsenate [As (V)]. Otte et al. (1991) showed that iron plaque played an important role in mediating As accumulation in the salt marsh plant Aster tripolium. Although the role of iron plaque on roots has been investigated in recent years, the relationship between iron plaque and As accumulation in plants is still unclear.
In rice plants, iron plaque can be formed both under natural and laboratory conditions (Chen et al., 1980; Greipsson and Crowder, 1992; Greipsson, 1994, 1995). Its role may be important for the development of practical approaches to reducing As accumulation. A previous experiment showed that iron plaque had a very strong affinity to arsenate and enhanced As uptake, but reduced translocation from roots to shoots (Liu et al., 2004). The aim of this work was to investigate the effect of different amounts of iron plaque on arsenate uptake and translocation, and to understand the interactions between Fe and As. In addition, the differences between genotypes in the formation of iron plaque, and in arsenate uptake and translocation were also investigated.
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Materials and methods |
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Experimental conditions
The experiment was carried out in a controlled environment growth chamber with a 14 h light period (260–350 mmol m–2 s–1). The temperature was kept at 25 °C during the day and 20 °C during the night. The relative humidity was 70%.
Preparation of rice seedlings
Seeds of three rice (Oryza sativa L.) cultivars, Gold 23A, Jinyou22, and CDR22 (a hybrid group, Gold 23A and CDR22 are the parents, Jinyou22 is the offspring) were obtained from Professor Li Damo, Institute of Subtropical Regional Agriculture, Chinese Academy of Sciences. Seeds were sterilized in 30% H2O2 solution for 15 min followed by thorough washing with deionized water. The seeds were germinated in moist perlite. After 3 weeks, uniform seedlings were selected and transplanted to PVC pots (7.5 cm diameter and 14 cm height, one plant per pot) containing 500 ml 1/3 strength nutrient solution, modified from Hewitt (1966) as shown in Table 1. The entire nutrient solution was changed twice per week, and the solution pH value was adjusted to 5.5 using 0.1 M KOH or HCl.
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Experimental treatments
After 3 weeks, iron plaque was induced on the roots as follows. Prior to iron plaque induction, all seedlings were put into deionized water for 12 h to minimize any interference from other elements with iron. They were then transferred into 500 ml solution with 20, 40, 60, 80, and 100 mg l–1 of ferrous ion for 24 h (Fe2+ as FeSO4.7H2O), and these treatments were therefore called Fe20, Fe40, Fe60, Fe80, and Fe100, respectively. Solution pH was adjusted to 5.5 using 0.1 M KOH or HCl. Seedlings were subsequently grown in nutrient solution for 2 d, before exposure to arsenic.
After iron plaque was induced, seedlings were allowed to grow in 1/3 strength normal nutrient solution for 2 d. Plants were then grown in solution with 0.5 mg As l–1 as Na3AsO4.12H2O for 10 d. The As concentration of 0.5 mg l–1 was chosen because a preliminary experiment showed that this dose did not cause acute toxicity to the rice seedlings. It was comparable to some contaminated irrigation water, and was lower than the highest As-contaminated irrigation water (2 mg As l–1) in some areas (Tondel et al., 1999; Abedin et al., 2002b). Each treatment had four replicates, and there were 60 pots in total.
Measurement of growth response and DCB extraction of iron plaque from roots
At harvest, iron plaque on fresh root surfaces was extracted using dithionite-citrate-bicarbonate (DCB) using the method of Taylor and Crowder (1983b) and Otte et al. (1991). The whole root system of each seedling was incubated for 60 min at room temperature (20–25 °C) in 40 ml of a solution containing 0.03 M sodium citrate (Na3C6H5O7.2H2O) and 0.125 M sodium bicarbonate (NaHCO3), with the addition of 0.6 g sodium dithionite (Na2S2O4). Roots were rinsed three times with deionized water that was added to the DCB-extracts. The resulting solution was made up to 100 ml with deionized water. After DCB extraction, roots and shoots were oven-dried at 70 °C for 3 d and weighed.
Plant analysis
Dried plant material was ground and about 0.25 g weighed accurately into clean, dry digestion tubes (100 ml) (FOSS digestion tubes). Concentrated HNO3 (5 ml) was added and allowed to stand overnight. On the following day, the tubes were placed on a heating block (2006 Digestion System of FOSS TECATOR) and the temperature was raised to 80 °C for 1 h and then to 120–130 °C for 20 h. A reagent blank and standard reference plant material (GBW07605 from the National Research Center for Standard Materials in China) were included, to verify the accuracy and precision of the digestion procedure and subsequent analysis. After digestion the solutions were cooled, diluted to 50 ml with ultra-pure water (Easy-pure, Dubugue, Iowa, USA) and filtered into acid-washed plastic bottles. The concentrations of Fe and As in the DCB-extracts and in the acid digests were measured by an inductively coupled plasma-optical emission spectrometer (ICP-OES, Optima 2000 DV, Perkin Elmer, USA) and atomic fluorescence spectrometry (AF-610A, Beijing Ruili Analytical Instrument Co., Beijing, China), respectively. An internal standard was included and negligible matrix effect was observed for both ICP-OES and atomic fluorescence spectrometry.
Data analysis
Element concentrations in DCB extracts, roots and shoots were calculated on the basis of dry weight. Total As (TAs), percentages of As in DCB extracts, roots and shoots were calculated as follows:
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Statistical analysis
Analysis of variance (ANOVA) on plant biomass and concentrations of metals was performed using Windows-based Genstat (6th edn, NAG Ltd, England). Tukey's multiple comparison test was carried out according to the LSD (least significance difference) values.
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Results |
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Plant growth
Fe2+ in pretreatment solutions and 0.5 mg As l–1 in treatment solutions after iron plaque induction had no effects on the growth of rice plants (Table 2). However, there were significant differences in biomass of roots and shoots between genotypes (P<0.001) with the ranking of Gold 23 A> CDR22
Jinyou22.
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Formation of iron plaque and Fe uptake and translocation
Iron plaque was clearly visible as a reddish coating on the root surface after 12 h of pretreatment with Fe2+. The Fe amounts in the iron plaque formed were different between genotypes (Fig. 1). The Fe amounts in the iron plaque were positively correlated with Fe2+ concentrations in solutions for Gold 23A and Jinyou22 (linear relationship, r=0.96, P<0.001 and r=0.89, P=0.045, respectively). For genotype CDR22, the amount of Fe in plaque increased above Fe20, but there was no linear relationship between Fe amounts in the iron plaque and the Fe2+ concentrations in the pretreatment solutions (r=0.55, P=0.336).
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The Fe concentrations in roots increased significantly with increasing Fe2+ concentrations in the pretreatment solutions (Table 3, P<0.001). For genotype Gold 23A, Fe concentrations in the shoots increased significantly with increasing Fe2+ concentrations in the pretreatment solutions; for genotype Jinyou22 Fe concentrations in the shoots firstly increased and then decreased at Fe100 and those for genotype CDR22 were not affected by Fe concentrations in the pretreatment solutions (Table 3).
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Effects of iron plaque on As uptake and translocation
Arsenic concentrations in DCB extracts (and assumed to be in iron plaque) increased significantly with increasing Fe amounts in iron plaque for the three genotypes (r=0.88, n=15, P<0.001) (Fig. 2). Both Fe2+ concentrations in the pretreatment solutions and genotypes had significant effects on As concentration in iron plaques (P<0.01).
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Arsenic concentrations in roots showed no significant differences between cultivars, but those in shoots did show significant differences between cultivars, with the following ranking: CDR22> Jinyou22 >Gold23A (Table 4). Arsenic concentrations in the roots increased significantly at Fe100 for Jinyou22 and CDR22. However, Fe2+ concentrations in the pretreatment solutions had no significant effect on As concentrations in the roots for Gold23A and on As concentrations in the shoots for all cultivars. In addition, shoot As concentrations were positively correlated with shoot iron concentrations (r=0.78, n=15, P< 0.01, Fig. 3).
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0.001).Arsenic distribution in different plant components
Arsenic in DCB extracts was significantly higher than that in roots and shoots (Table 5), and accounted for up to 75–89% of the total As. There were no significant differences in percentage of As in DCB extracts between genotypes. However, there were significant differences between genotypes for the percentages of As distributed in roots (P<0.001) and shoots (P<0.05).
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
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The results showed that Fe concentrations in pretreatment solutions to induce plaque had no significant effect on the growth of rice plants grown in nutrient solution with 0.5 mg As l–1 (Table 2). This agrees with results obtained by Ye et al. (1997
, 2001), but differed from those of Christensen and Sand-Jensen (1998). Greipsson and Crowder (1992) and Greipsson (1994, 1995) suggested that the formation of iron plaque could enhance the growth of plants and reduce excessive Cu, Ni, and Zn toxicity in rice seedlings. In this experiment, the variation in the amounts of iron plaque induced was relatively small.
The DCB-extracted As on the root surfaces correlated significantly with the amounts of iron plaque on the root surface for the three genotypes (Fig. 2). This result strongly suggests that As in DCB extracts is, in fact, strongly associated with iron plaque as observed in the previous study (Liu et al., 2004) and was similar to other plant species (St-Cyr and Crowder, 1990; Greipsson, 1994, 1995). Field investigation showed that As concentrations in DCB extracts of Aster tripolium were about 40 times higher in the flooded treatment than in the aerated treatment (Otte et al., 1991). Zhang et al. (1998, 1999) reported that iron plaque on rice roots could accumulate zinc and phosphorus from the growth medium, and Ye et al. (1997, 2001) also found that Cu concentrations on the root surface of Typha latifolia with iron plaque were significantly higher than on those without iron plaque. The present study showed that the As, that was assumed to be associated with iron plaque, accounted for up to 75–89% of total As, which was much higher than those reported for Cu and Ni in Typha latifolia (30–40%; Ye et al., 1997). This indicated that the sequestration capacity of iron plaque may be different between cations and anions.
A number of reports have shown that iron plaque can act as a barrier to the uptake of toxic metals (Greipsson, 1994, 1995; Otte et al., 1991; Zhang et al., 1998; Christensen and Sand-Jensen, 1998; Batty et al., 2000) or alternatively, as a pool that increases the uptake of toxic and nutrient elements (Zhang et al., 1998, 1999; Ye et al., 2001). Some authors have already suggested that the overall effect of iron plaque on the uptake of nutrient and/or toxic elements may depend on the amounts (thickness) of iron plaque on the roots (Zhang et al., 1998, 1999; Otte et al., 1989). Otte et al. (1989) demonstrated that zinc concentrations in roots of Aster tripolium were significantly higher in roots with 500-2000 nmol Fe cm–2 on the root surface compared to those with less than 500 or more than 2000 nmol Fe cm–2. However, in the present study, the effect of iron plaque on arsenic uptake did not follow this trend, which may be due to the fact that phosphorus and zinc sequestration in the iron plaque is altered mainly through adsorption or co-precipitation. In the case of As, redox reaction may also occur and result in different As species in the iron plaque, such as arsenate and arsenite. In other words, the mechanisms involved in the interactions of zinc, phosphorus, and arsenic with iron plaque are different.
Despite the fact that increasing amounts of iron plaque increased As accumulation on the root surface, they did not affect As concentrations in rice shoots, which indicated that iron plaque may act as a ‘buffer’ to prevent increased As translocation from roots to shoots. Therefore, the formation of iron plaque could alter the arsenic accumulation in the above-ground parts of rice plants. This agrees with previous findings for As uptake by rice (Liu et al., 2004) and the uptake of As and other metals by other plant species (Otte et al., 1989; Greipsson and Crowder, 1992; Greipsson, 1994; Ye et al., 1998, 2001; Christensen and Sand-Jensen, 1998; Batty et al., 2000). Nevertheless, the role of iron plaque in altering the translocation of nutrients or toxic metals may depend on the plant species and the ionic species involved. For example, Ye et al. (1997) showed that iron plaque increased Ni translocation in Typha latifolia. Zhang et al. (1999) reported that P concentrations in shoots of rice plants with iron plaque were higher than those without plaque. For further understanding of the role of iron plaque in altering As uptake by rice, studies with soil and nutrient solution culture are needed to investigate the composition and translocation of As in rice plants and how As interacts with Fe in plaques in roots and in shoots with some microscopic techniques, such as scanning electron microscopy and synchrotron radiation.
The results also showed that there is considerable difference in the As concentrations in the shoots of the three cultivars tested; cultivar Gold23A contained roughly half of the As in the shoots compared with cultivar CDR22 (Table 4). Arsenic accumulation in the shoots has a direct relevance to As transfer in the food chains, and thus to the health risks posed upon the populations that consume rice and the products of livestock fed with rice straw produced from contaminated areas. It is likely that a cultivar with relatively less As accumulation in the shoots would probably have less As accumulation in the grains. Given the wide range of As contamination in paddy soils in South-East Asia (Dey et al., 1996; Abedin et al., 2002a; Nickson et al., 1998; Chowdhury et al., 1999, 2000; Xie and Huang, 1998; Ullah, 1998; Alam and Sattar, 2000), strategies to reduce the transfer of As from soil to edible parts of crop plants deserve further attention. The large genotypic difference in As accumulation in shoots observed in this study certainly encourages future programmes to screen and/or breed rice cultivars with low As accumulation in shoots (and possibly in grains).
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Conclusion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
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These results demonstrated that the arsenic accumulated on the root surface was largely associated with iron plaque. However, As concentrations in the shoots were not altered by changes in the amounts of iron plaque, although the changes were quite small in two of the genotypes. Overall, the results suggested that iron plaque may act as a ‘buffer’ preventing the increased translocation of As to shoots. The large genotypic variation in shoot As concentrations encourage endeavours to breed new rice cultivars with low As accumulation for areas with As contamination.
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Acknowledgements |
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The work was financially supported by the Ministry of Science and Technology of China (2002CB410808), the Natural Science Foundation of China (40225002 and 30370821), and the Chinese Academy of Sciences (Hundred Talent Program).
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