Do phosphorus nutrition and iron plaque alter arsenate. (As) uptake by rice seedlings in hydroponic culture?

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1 Research Do phosphorus nutrition and iron plaque alter arsenate Blackwell Publishing, Ltd. (As) uptake by rice seedlings in hydroponic culture? W.-J. Liu 1,2, Y.-G. Zhu 1,3, F. A. Smith 3 and S. E. Smith 3 1 Research Center for Eco-environmental Sciences, Chinese Academy of Sciences, China; 2 College of Natural Resources and Environment, Hebei Agricultural University, Baoding, Hebei Province, China; 3 Soil and Land Systems, School of Environmental Sciences, The University of Adelaide, Adelaide, South Australia, 5005, Australia Summary Author for correspondence: Y.-G. Zhu Tel: Fax: Received: 19 October 2003 Accepted: 19 December 2003 doi: /j x A hydroponic experiment was conducted to investigate the effect of phosphorus (P) nutrition and iron plaque on root surfaces on arsenate uptake by, and translocation within, the seedlings of three cultivars of rice (Oryza sativa). Supply of 0.5 mg As l 1 had no significant effects on dry weights of shoots or roots, but resulted in elevated concentrations of As in tissues, particularly in roots. Rice roots appeared reddish after 24 h in P solution (without P), indicating the formation of iron plaque. Arsenic concentrations in iron plaque (determined in dithionite citrate bicarbonate (DCB)-extracts) were significantly higher in P plants (up to 1180 mg kg 1 in cultivar ) than in +P plants. Concentrations of arsenic in shoots were significantly lower in P plants than in +P plants. This indicates that iron plaque might sequestrate As, and consequently reduce the translocation of arsenic from roots to shoots. Values for the total uptake of As show that As in P rice plants was mainly concentrated in the DCB-extracts or on the surface of rice roots, whereas most arsenic in +P plants was accumulated in the roots. Arsenic significantly decreased the concentrations of iron (Fe) in roots and shoots (P < 0.001) and slightly reduced P concentrations in shoots, except for the P cultivar. Key words: arsenic, rice (Oryza sativa), iron plaque, phosphorus, uptake. New Phytologist (2004) 162: Introduction Arsenic (As) is a toxic and carcinogenic element that occurs widely in soil environments around the world. Soil contamination with As occurs through both natural and anthropogenic pathways. Irrigation of agricultural land with As-contaminated wastewater or groundwater, particularly in Bangladesh, India and south-east Asia, can cause the accumulation of As in both soils and plants, posing risks to soil ecosystems and human health (Marin et al., 1992; Xie & Huang, 1998; Meharg & Rahman, 2003). A recent study indicated that the concentration of As in rice straw could be up to 92 mg kg 1, when rice plants were irrigated with As-contaminated groundwater (Abedin et al., 2002b). However, in many countries the legal limit for straw fed to cattle is 0.2 mg kg 1 (Nicholson et al., 1999). Accumulated As in plants and animals can eventually be transferred to human beings, causing health problems. Arsenic exists in the environment in both inorganic and organic forms, and both arsenite and arsenate are often found in both anaerobic and aerobic soil environments. Arsenate is an analogue of phosphate, competing for the same sorption sites in the root apoplast and for the same uptake carriers in the root plasmalemma (Meharg & Macnair, 1992; Meharg & Hartley-Whitaker, 2002). Phosphate can decrease or increase the uptake of As by plants, depending on the speciation of As, the species of plant and the plant growth medium (Tsutsumi, 1980; Otte et al., 1990). In addition, the bioavailability of As in soil is usually affected by physico-chemical properties of iron (Fe); Fe (hydro-) oxide has a high affinity for adsorption of As in soil (Belzile & Tessier, 1990; Jain et al., 1999). New Phytologist (2004) 162:

2 482 Research Nonetheless, there are few reports on the effects of interactions between arsenate, phosphate and iron hydroxides/oxides on As behavior in soil plant systems. Iron plaque is commonly formed on the surfaces of roots of aquatic plants, including Oryza sativa, Typha latifolia and Phragmites communis, and is mainly caused by the oxidation of ferrous to ferric iron and the precipitation iron oxide on the root surface (Armstrong, 1964), promoted by the release of oxygen and oxidants into the rhizosphere (Armstrong, 1967; Chen et al., 1980, Taylor & Crowder, 1983; Taylor et al., 1984). Iron plaque may be amorphous or crystalline, in the forms of ferric hydroxides, goethite and lepidocrocite (Bacha & Hossner, 1977; Chen et al., 1980). A recent study showed that iron plaque is composed dominantly of ferrihydrite (63%) with lesser amounts of goethite (32%) and minor level of siderite (5%) (Hansel et al., 2001). Iron oxides or hydroxides have high affinity for As in soils and other environments (Belzile et al., 1990). Meng et al. (2002) found that As (V) had very strong binding affinity for iron hydroxides. Otte et al. (1991) showed that iron plaque played an important role in the uptake of As by salt-marsh plants, but there is little information on its role in As uptake by rice or other aquatic food plants. In our preliminary experiments, iron plaque was induced onto the roots of rice plants grown under P starvation in solution culture, suggesting the possibility of three-way interactions between arsenate and phosphate supply and iron plaque development in arsenate uptake by rice. The aim of this study was to investigate the effects of P starvation and iron plaque induced by P starvation on arsenate uptake by rice in solution culture. Materials and Methods Preparation of rice seedlings Seeds of three rice (Oryza sativa L.) cultivars,, and were obtained from Professor Li Damo, Institute of Subtropical Regional Agriculture, Chinese Academy of Sciences. Seeds were disinfected in 30% H 2 O 2 (wt : wt) solution for 15 min, followed by thorough washing with deionized water. The seeds were germinated in moist Perlite. After 3 wk, uniform seedlings were selected and transplanted to PVC pots (7.5 cm diameter and 14 cm high, one plant per pot) containing 500 ml nutrient solution. The composition of P nutrient solution was as follows: 4.4 mm NH 4 NO 3, 2 mm K 2 SO 4, 4 mm CaCl 2, 1.5 mm MgSO 4, 1.4 mm KNO 3, 50 µm Fe(II)- ethylenediaminetetraacetic acid (EDTA), 10 µm H 3 BO 4, 1.0 µm ZnSO 4, 1.0 µm CuSO 4, 5.0 µm MnSO 4, 0.5 µm Na 2 MoO 4, 0.2 µm CoSO 4 7H 2 O. For the +P treatment, 4.4 mm NH 4 NO 3, 1.4 mm KNO 3 in P nutrient solution were replaced by 5 mm NH 4 NO 3, and 1.3 mm KH 2 PO 4 was added into the solution; other compounds were the same as in the P solution. The composition was modified from that of Hewitt (1966). All nutrient solutions were changed twice per week, and ph was adjusted to 5.5 using 0.1 M KOH or HCl. Iron in the growth solution was supplied as Fe 2+ to represent the main iron species in paddy soil solution. Treatments The solution culture experiment was carried out in three stages. At stage I, all seedlings were grown in full nutrient solution (+ P) for 1 wk. At stage II, half of the seedlings were rinsed three times with deionized water and transferred to pots containing 500 ml nutrient solution without phosphorus ( P), and the remaining seedlings were grown in +P solution. This stage lasted 10 d. Stage III, +P and P seedlings were each divided into two groups and grown for a further 10 d in the same nutrient solutions with 0.5 mg As l 1 as Na 3 AsO 4 12H 2 O (+As) or without As ( As). Thus, there were four treatments for the three cultivars (+P +As, +P As, P +As and P As), each replicated three times to give a total of 36 pots. The nutrient solution was not aerated during the experimental period to mimic the anaerobic conditions. Growth conditions The experiment was carried out in a controlled environment growth chamber with a 14-h light period ( µe m 2 s 1 ) and temperatures of 28 C day and 20 C night. The relative humidity was 70%. The plants were harvested 48 d after germination. Growth of rice seedlings and DCB extraction of iron plaque At harvest, iron plaque on fresh root surfaces was extracted using dithionite citrate bicarbonate (DCB) using the method of (Taylor & Crowder 1983) and Otte et al. (1991). The whole root system of each seedling was incubated for 60 min at room temperature (20 25 C) in 30 ml of a solution containing 0.03 M sodium citrate (Na 3 C 6 H 5 O 7 2H 2 O) and M sodium bicarbonate (NaHCO 3 ), with the addition of 0.6 g sodium dithionite (Na 2 S 2 O 4 ). Roots were rinsed three times with deionized water that was added to the DCB extract. The resulting solution was made up to 50 ml with deionized water. After DCB extraction, roots and shoots were oven dried at 70 C for 3 d and weighed. Tissue elements analysis Dried plant material was ground and about 0.25 g weighed accurately into clean, dry digestion tubes (100 ml) (FOSS, Tecator AB, Sweden). Concentrated HNO 3 (5 ml) was added and allowed to stand overnight. The following day, the tubes were placed on a digestor (2040 Digestion System of FOSS TECATOR) and the temperature was raised to 80 C for 1 h and then controlled at C for 20 h to avoid As New Phytologist (2004) 162:

3 Research 483 volatilization. A reagent blank and a standard reference plant material (GBW07605 from the National Research Center for Standards 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, Dubuque, IA, USA) and filtered into acid-washed plastic bottles. The concentrations of As, P, Fe, manganese (Mn), copper (Cu) and zinc (Zn) in the DCBextract and in the acid digests were measured by ICP-MS (Agilent-7500, Agilent Technologies Co. Ltd, Palo Alto, CA, USA). Data analysis Element concentrations in DCB extracts, roots and shoots were calculated on the basis of dry weight. Total As uptake (T As ), percentages of As in DCB-extracts, roots and shoots were calculated as follows: T As = T DCB-extract-As + T Root-As + T Shoot-As T DCB-extract-As = C DCB-extract-As Roots biomass (T DCB-extract-As, T Root-As and T Shoot-As represent the total As in DCB-extracts, roots and shoots, respectively; C DCB-extract-As, C Root-As and C Shoot-As are As concentrations in DCB-extracts, roots and shoots, respectively). Statistical analysis Analysis of variance (ANOVA) on plant biomass and concentrations of nutrients and metals were performed using Windowsbased GENSTAT (6th edition, NAG Ltd Oxford, UK). Results Plant growth. After 24 h in the P treatments rice roots appeared reddish, indicating the formation of iron plaque, but in the +P treatments they remained white. Low P supply ( P) significantly reduced shoot biomass of rice seedlings except for, compared with +P plants, regardless of As treatment, but did not have significant effects on root biomass (Table 1). There was a significant difference in shoot biomass between cultivars with the ranking of < <. However, supply of 0.5 mg As l 1 had no significant effects on dry weights of shoots or roots. T Root-As = C Root-As Roots biomass T Shoot-As = C Shoot-As Shoots biomass DCB-As% = (T DCB-extract-As /T As ) 100 Root-As% = (T Root-As /T As ) 100 Shoot-As% = (T Shoot-As /T As ) 100 Uptake and translocation of As, Fe and P Arsenic concentrations were under detection limits in plants grown without As addition (results not shown). Concentrations of As in DCB extracts, and roots and shoots for +As plants are shown in Fig. 1 and statistical analyses in Table 2. Concentrations of As in DCB-extracts in P plants were significantly higher than those in +P plants ( 598 mg kg 1 vs. Table 1 Biomass (g per pot, dry wt) of rice (Oryza sativa) seedlings of three cultivars exposed to 0.5 mg l 1 arsenic (+As) and without arsenic ( As), with phosphorus (+P) and without phosphorus ( P) in nutrient solution Shoot Root Cultivars Treatment As +As As +As +P 0.41 ± ± ± ± 0.02 P 0.41 ± ± ± ± P 0.50 ± ± ± ± 0.02 P 0.41 ± ± ± ± P 0.63 ± ± ± ± 0.01 P 0.56 ± ± ± ± 0.01 Analysis of variance As ns ns Cultivars (C) P < ns P P = ns As C ns ns As P ns ns C P P = P < As C P ns ns Data are means ± SE; n = 3. New Phytologist (2004) 162:

4 484 Research Table 2 Analysis of variance (three-way ANOVA) on arsenic (As) concentrations in dithionite citrate bicarbonate (DCB) extracts, roots and shoots of three rice (Oryza sativa) cultivars shown in Fig. 1 DCB-As Root-As Shoot-As As < < < Cultivars (C) P = NS < Phosphorus (P) < P = < As C P = ns < As P < P = < C P P = ns ns As C P P = ns ns Fig. 1 Arsenic (As) concentrations in dithionite citrate bicarbonate (DCB) extracts (a), roots, (b), and shoots of three rice (Oryza sativa) cultivars (, and ) of phosphorus (P) starved (open columns) and nonstarved (closed columns) plants, exposed to 0.5 mg As l 1 (mean SE; n = 3). 53 mg kg 1 ; 1179 mg kg 1 vs. 48 mg kg 1 ; mg kg 1 vs. 47 mg kg 1, respectively) (Fig. 1a). Concentrations of As in roots of P plants were significantly higher than those in +P plants, but the difference was much smaller than for As concentrations in DCB extracts (Fig. 1b). Unlike As concentrations in DCB-extracts and roots, the concentrations of As in shoots were significantly lower in P plants than those in +P plants (Fig. 1c). For P plants, concentrations of As were in the following ranking, DCB-extract-As > Root-As > Shoot-As, while for +P plants, concentrations of As followed the trend Root-As > DCBextract-As > Shoot-As. Concentrations of As in DCBextracts and shoots also showed significant differences between cultivars, but not in roots. Cultivar had the highest As concentrations in DCB-extracts, and cv. had the lowest As concentrations in shoots. The total uptake of As in P +As rice seedlings ( µg; µg; and µg) was significantly higher than in +P +As seedlings ( µg; µg; µg) (Table 3). In seedlings grown with P, most As accumulated in the roots and shoots. However, in seedlings grown without P, As accumulated mainly in the DCB extracts (that is, in the iron plaque formed on surface of rice roots) (Table 3). In P +As plants, only % of the total As was taken up by the plants, but in +P +As plants, 15 23% total As was transported to shoots. The P concentrations in DCB extracts, roots and shoots of seedlings in P treatments were significantly lower than those of the seedlings in +P treatments (Table 4). P concentrations in both +P and P treatments showed the following trend: Shoot-P > Root-P > DCB-P. Cultivars and exposure to As had no significant effect on P concentrations in DCB-extracts or roots, but reduced P concentrations in shoots slightly, with the exception of P plants of cv.. Despite the formation of iron plaque on root surfaces in P treatments there were no significant effects on DCBextractable iron (Table 4). Exposure to As significantly decreased the concentrations of Fe in roots and shoots (P < 0.001). The highest Fe concentration in root was observed in the P-As treatment for (650 mg Fe kg 1, Table 5); the highest Fe concentration in shoot was observed in cv. (563 mg Fe kg 1 ). Uptake and translocation of Mn, Cu, Zn The concentrations of Mn, Cu, Zn in roots and Mn concentrations in shoots decreased significantly in P treatments but no effect was observed on Cu, Zn concentrations in shoots New Phytologist (2004) 162:

5 Research 485 Table 3 Total uptake of arsenic (As) and the percentages in different components with phosphorus (+P) and without phosphorus ( P) treatments for three rice (Oryza sativa) cultivars, following As exposure Cultivar/treatment Total uptake (µg) DCB-As% Root-As% Shoot-As% +P 62.5 ± ± ± ± 1.2 P 227 ± ± ± ± 0.1 +P 62.0 ± ± ± ± 0.4 P 232 ± ± ± ± 0.2 +P 56.9 ± ± ± ± 1.9 P 169 ± ± ± ± 1.1 Analysis of variance Cultivars (C) P = 0.01 ns P = P = P < < < < P C P = ns ns P = Data are means ± SE. DCB, dithionite citrate bicarbonate. (Table 5). Exposure to As had no effect on Mn concentrations in roots but significantly decreased concentrations in shoots. The effects of As on Zn concentrations in roots and shoots were the opposite to those on Mn. The Cu concentrations in both roots and shoots were significantly decreased in seedlings exposed to As. Discussion Hydroponic culture is a realistic way to investigate effects of P and As supply on rice because it is an aquatic plant, and in the culture system no aeration was supplied to simulate the anaerobic conditions. Our results are therefore relevant to normal cultivation of inundated rice. Similar experimental protocols have also been used to investigate the role of iron plaque in plant accumulation of nutrients (Zhang et al., 1998, 1999) and heavy metals (Ye et al., 2001). The reported effects of As accumulation in rice on growth of plants are inconclusive. We found no significant decrease in dry weights of shoots or roots of rice exposed to 0.5 mg As l 1 for 10 d under hydroponic conditions (Table 2). This is consistent with the results of Tsutsumi (1980), who observed no differences in height of rice plants grown in soil with As concentrations lower than 125 mg kg 1. By contrast, there are number of reports of reduction in growth following As application to rice and other plants. For example, increasing As concentrations (up to 8 mg l 1 ) in irrigation water significantly decreased plant height, root biomass and grain yield in rice, but did not significantly reduce straw yield (Abedin et al., 2002a,b). We found that iron plaque developed on rice roots 24 h after transfer to P treatments. This suggested that rice plants have an adaptive metabolic reaction to the condition of P deficiency, which is consistent with previous work. Kirk & Du (1997) found that P deficiency resulted in an increase in oxygen release from rice roots, which would have had the effect of stimulating iron plaque formation. In our experiment, P starvation was used to manipulate the P nutrition of rice plants grown in solution culture. Although P concentrations in P plants were significantly lower than those in +P plants, the P concentrations in P plants were not at deficiency levels (Table 5). Based on the information obtained thus far, it is still not clear whether external or internal P concentrations control the stimulation of the formation of iron plaque. Nevertheless, our results showed that iron plaque has very strong binding affinity to As in the solution, with concentrations in DCB extracts in P plants times higher than those in +P plants of all three cultivars. This is in line with the observation that iron plaque formed on the roots of the salt-marsh plant Aster tripolium could accumulate As (Otte et al., 1991). Arsenate acts as a phosphate analog, and is taken up by plants via P transporter systems (Asher & Reay, 1979; Macnair & Cumbes, 1987; Meharg & Macnair, 1992). Deficiency or starvation of P can enhance arsenate uptake and accumulation by barley (Lee, 1982), grasses (e.g. Holcus lanatus) (Meharg & Macnair, 1992), and even in the As hyperaccumulator fern Pteris vittata (Wang et al., 2002). In rice plants, in the present experiment, P starvation reduced the translocation of As to the shoots, this might be a result of As sequestration in iron plaque induced by P starvation in the growth solution. One may also argue that the reduced As translocation is caused by slow shoot growth under P starvation, since As concentrations in roots were enhanced by P starvation. However, the observed As concentrations in roots in P plants may be partly ascribed to residue of As bound to iron plaque after DCB extraction, since it is unlikely to be 100% complete, particularly given that fact that As concentrations in DCB extracts were so high (Fig. 1). Nevertheless, using intact rice roots, this is, to our knowledge, the first observation of a possible three-way interaction between P nutrition, iron plaque formation and As uptake by plants. Our results demonstrate that by exploiting the effects of iron plaque in binding As, it is possible to reduce the transfer of As from soils to rice. The common formation of iron plaque by rice, including the three cultivars we used, means that the effect could be widely applied. Furthermore, New Phytologist (2004) 162:

6 486 Research Table 4 Iron (Fe) and phosphorus (P) concentrations in dithionite-citrate-bicarbonate (DCB) extracts, roots and shoots with (+P) and without P ( P) treatments for three rice (Oryza sativa) cultivars, following arsenic (As) exposure (+As) and without As exposure ( As) Fe (mg kg 1 ) P (mg kg 1 ) Treatment/cultivar As +As As +As DCB extracts +P ± ± ± ± 671 P 7969 ± ± ± ± 51 +P ± ± ± ± 710 P ± ± ± ± 85 +P ± ± ± ± 231 P 9270 ± ± ± ± 66 Roots +P 438 ± ± ± ± 393 P 548 ± ± ± ± 61 +P 420 ± ± ± ± 571 P 445 ± ± ± ± 16 +P 501 ± ± ± ± 351 P 650 ± ± ± ± 149 Shoots Gold 23 A +P 534 ± ± ± ± 643 P 563 ± ± ± ± 230 +P 527 ± ± ± ± 984 P 523 ± ± ± ± 203 +P 380 ± ± ± ± 855 P 365 ± ± ± ± 188 Analysis of variance DCB-extracts Root Shoot Fe P Fe P Fe P As NS ns < NS < P = Cultivars (C) P = ns < ns < < P NS < < < ns < As C NS ns ns ns ns ns As P NS ns ns ns ns P = C P P = ns ns ns ns < As C P ns ns ns ns ns ns Data are means ± SE. DCB, dithionite citrate bicarbonate. iron plaque may be also responsible for the oxidation of arsenite to arsenate. Arsenite is much more toxic than arsenate. X- ray fluorescence microtomography showed that As bound to iron plaque on root surfaces of the aquatic plants Phalaris arundinacea and Typha latifolia was largely arsenate (Hansel et al., 2002). Therefore, iron plaque may also play a role in reducing the toxicity of As contamination in soil plant systems. In this experiment, both P and +P plants were supplied with the same amounts of Fe in the nutrient solution. However, the difference in Fe concentrations in DCB extracts between the P treatments was much smaller than expected (Table 5), despite the significant appearance of iron plaque on the root surface of P plants. This might be explained if P rice plants release more O 2 and oxidants from roots (Kirk & Du, 1997), which causes the oxidation of Fe(II) to ferric oxide or hydroxide forming iron plaque on the root surface and even in the root apoplast. By contrast, if +P plants release less O 2 they might not form iron plaque. These plants may New Phytologist (2004) 162:

7 Research 487 Table 5 Manganese (Mn), copper (Cu) and zinc (Zn) concentrations in roots and shoots with phosphorus (+P) and without phosphorus ( P) treatments for three rice (Oryza sativa) cultivars (, and ), following arsenic (As) exposure (+As) and without As exposure ( As) Mn (mg kg 1 ) Cu (mg kg 1 ) Zn (mg kg 1 ) Treatments/cultivar As +As As +As As +As Shoots +P 1255 ± ± ± ± ± ± 7.8 P 624 ± ± ± ± ± ± 1.9 +P 1157 ± ± ± ± ± ± 9.3 P 561 ± ± ± ± ± ± 4.6 +P 807 ± ± ± ± ± ± 21.1 P 581 ± ± ± ± ± ± 3.2 Roots +P 108 ± ± ± ± ± ± 15.1 P 56.9 ± ± ± ± ± ± 2.1 +P 77.0 ± ± ± ± ± ± 4.4 P 43.6 ± ± ± ± ± ± 7.3 +P 109 ± ± ± ± ± ± 3.3 P 72.9 ± ± ± ± ± ± 4.2 Analysis of variance Root Shoot Mn Cu Zn Mn Cu Zn As NS < P = P = 0.01 < NS Cultivars (C) P = NS < < < NS P < < < < NS NS As C NS NS NS NS NS NS As P P = < NS NS NS NS C P NS NS < < NS NS As C P NS NS NS P = NS NS Data are means ± SE. normally take up Fe as Fe(II) from solution, adsorb ferrous iron on the root surface and accumulate ferric iron in the root apoplast. Apoplastic Fe would also be extracted by DCB solution, and our method is similar to those used in estimating apoplastic Fe (Strasser et al., 1999). It is possible that P nutrition may affect the distribution of iron between root surface and apoplastic free space in roots, but this needs further study. Our results go some way to understanding the role of P nutrition and iron plaque in controlling the concentrations of As in rice shoots and, with further work, may form the basis of management practices to alleviate As accumulation to toxic levels. The different rice cultivars had different capacities to form iron plaque on root surfaces. It is therefore possible to control As uptake by rice through the selection of rice genotypes with better oxidizing capacity and therefore higher capacity to form iron plaque, and the management of P nutrition for optimal formation of iron plaque. The concentration of P in paddy soils varies greatly with soil type and fertilizer application. In a pot experiment with addition of 100 mg per kg soil, Huguenin-Elle et al. (2003) found that the solution P concertration under flooded condition were around 0.03 mg l 1, and could be altered significantly by soil water content. In south-east China, Zhang et al. (2003) found that P concentrations in surface runoff (i.e. water on the paddy surface) varied from to 1.9 mg l 1 depending on soil types, growth seasons and P application rates. It is therefore possible to manipulate soil solution P through water and fertilizer management. Tissue P concentrations observed in our study (around 2 g kg 1 ) were not particularly low despite the P treatment, and biomass loss due to P treatment was not substantial. Thus, it is practical to manipulate New Phytologist (2004) 162:

8 488 Research iron plaque on rice root surface through the management of soil P. Acknowledgements We thank Prof. Li Damo (Institute of Subtropical Regional Agriculture, Chinese Academy of Sciences) for supplying rice seeds. This study was supported by the Natural Science Foundation of China ( ) and the Ministry of Science and Technology, China (2002CB410808). References Abedin MJ, Cotter-Howells J, Mehang AA. 2002a. Arsenic uptake and accumulation in rice (Oryza sativa L.) irrigated with contaminated water. Plant and Soil 240: Abedin J, Cresser M, Mehang AA, Feldmann J, Cotter-Howells J. 2002b. Arsenic accumulation and metabolism in rice (Oryza sativa L.). Environmental Science and Technology 36: Armstrong W Oxygen diffusion from the roots of some British bog plants. Nature 204: Armstrong W The oxidising activity of roots in water-logged soils. Physiologia Plantarom 20: Asher CJ, Reay PF Arsenic uptake by barley seedlings. Australian Journal of Plant Physiology 6: Bacha RE, Hossner LR Characteristics of coating formed on rice roots as affected by Fe and Mn additions. Soil Science Society of America Journal of 41: Belzile N, Tessier A Interactions between arsenic and iron oxyhydroxides in lacustrine sediments. Geochimca et Cosmochimca Acta 54: Chen CC, Dixon JB, Turner FT. 1980a. Iron coatings on rice roots: morphology and models of development. Soil Science Society of America Journal 44: Kirk GJD, Du VL Changes in rice root architecture, porosity, and oxygen and proton release under phosphorus deficiency. New Phytologist 135: Hansel CM, Fendorf S, Sutton S, Newville M Characterization of Fe plaque and associated metals on the roots of mine-waste impacted aquatic plants. Environmental Science and Technology 35: Hansel CM, La Force MJ, Fendorf S, Sutton S Spatial and temporal association of As and Fe species on aquatic plant roots. Environmental Science and Technology 36: Hewitt EJ Sand and water culture methods used in the study of plant nutrition, 2nd edn. Technical communication no. 22. Farnham Royal, UK: Commonwealth Agriculture Bureau. Huguenin-Elle O, Kirk GJD, Frossard E Phosphorus uptake by rice from soil that is flooded, drained or flooded then drained. European Journal of Soil Science 54: Jain A, Raven KP, Loeppert RH Arsenite and arsenate adsorption on ferrihydrite: surface charge reduction and net OH-1 release stoichiometry. Environmental Science Technology 33: Lee RB Selectivity and kinetics of ion uptake by barley plants following nutrient deficiency. Annals of Botany 50: Macnair MR, Cumbes Q Evidence that arsenic tolerance on Holcus lanatus L. is caused by an altered phosphate uptake system. New Phytologist 107: Marin AR, Masscheleyn PH, Patrick WH The influence of chemical form and concentration of arsenic on rice growth and tissue arsenic concentration. Plant and Soil 139: Meharg AA, Hartley-Whitaker J Arsenic uptake and metabolism in arsenic resistant and non-resistant plant species. New Phytologist 154: Meharg AA, Macnair MR Suppression of the high-affinity phosphate-uptake system-a mechanism of arsenate tolerance on Holcus lanatus L. Journal of Experimental Botany 43: Meharg AA, Rahman M Arsenic contamination of Bangladesh paddy soils: implication for rice contribution to arsenic consumption. Environmental Science and Technology 37: Meng XG, Korfiatis GP, Bang S, Bang KW Combined effects of anions on arsenic removal by iron hydroxides. Toxicology Letters 133: Nicholson FA, Chambers BJ, Williams JR, Unwin RJ Heavy metal contents of livestock feeds and animal manures in England and Wales. Bioresource Technology 70: Otte ML, Dekkers MJ, Rozema J, Broekman RA Uptake of arsenic by Aster tripolium in relation to rhizosphere oxidation. Canadian Journal of Botany 69: Otte ML, Rozema J, Beek MA, Kater BJ, Broekman RA Uptake of arsenic by estuarine plants and interactions with phosphate, in the field (Rhine estuary) and under outdoor experimental conditions. Science of the Total Environment 97/98: Strasser O, Kohl K, Romheld V Over-estimation of apoplastic Fe in roots of soil grown plants. Plant and Soil 210: Taylor GJ, Crowder AA Use of DCB technique for extraction of hydrous iron oxides from roots of wetland plants. America Journal of Botany 70: Taylor GJ, Crowder AA, Rodden R Formation and morphology of an iron plaque on the roots of Typha latifolia L. grown in solution culture. America Journal of Botany 71: Tsutsumi M Intensification of arsenic toxicity to paddy rice by hydrogen sulphide and ferrous iron I. Induction of bronzing and iron accumulation in rice by arsenic. Soil Science and Plant Nutrition 26: Wang JR, Zhao FJ, Meharg AA, Raab A, Feldmann J, McGrath SP Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics, interactions with phosphate, and arsenic speciation. Plant Physiology 130: Xie ZM, Huang CY Control of arsenic toxicity in rice plants grown on an arsenic-polluted paddy soil. Communications in Soil Science and Plant Analysis 29: Ye ZH, Cheung KC, Wong MH Copper uptake in Typha latifolia as affected by iron and manganese plaque on the root surface. Canadian Journal of Botany 79: Zhang HC, Cao ZH, Shen QR, Wong MH Effect of phosphate fertilizer application on phosphorus (P) losses from paddy soils in Taihu Lake Region 1. Effect of phosphate fertilizer rate on P losses from paddy soil. Chemosphere 50: Zhang X, Zhang F, Mao D Effect of Fe plaque outside roots on nutrient uptake by rice (Oryza sativa L.): zinc uptake. Plant and Soil 202: Zhang X, Zhang F, Mao D Effect of Fe plaque outside roots on nutrient uptake by rice (Oryza sativa L.): phosphorus uptake. Plant and Soil 209: New Phytologist (2004) 162:

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