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1 Environmentl Pollution 159 (211) 3739e3743 Contents lists ville t ScienceDirect Environmentl Pollution journl homepge: Phytoremedition of rsenic contminted pddy soils with Pteris vittt mrkedly reduces rsenic uptke y rice Wen-Ling Ye,, M. Asduzzmn Khn,c, Steve P. McGrth, Fng-Jie Zho, Rothmsted Reserch, Hrpenden, Hertfordshire AL5 2JQ, UK School of Erth nd Spce Sciences, University of Science nd Technology of Chin, Hefei, Anhui 2326, Chin c Sher-e-Bngl Agriculturl University, Sher-e-Bngl Ngr, Dhk-127, Bngldesh rticle info strct Article history: Received 23 Ferury 211 Received in revised form 11 July 211 Accepted 13 July 211 Keywords: Arsenic Arsenic specition Rice Phytoremedition Pteris vittt Arsenic (As) ccumultion in food crops such s rice is of mjor concern. To investigte whether phytoremedition cn reduce As uptke y rice, the As hyperccumultor Pteris vittt ws grown in five contminted pddy soils in pot experiment. Over 9-month period P. vittt removed 3.5e11.4% of the totl soil As, nd decresed phosphte-extrctle As nd soil pore wter As y 11e38% nd 18e77%, respectively. Rice grown following P. vittt hd significntly lower As concentrtions in strw nd grin, eing 17e82% nd 22e58% of those in the control, respectively. Phytoremedition lso resulted in significnt chnges in As specition in rice grin y gretly decresing the concentrtion of dimethylrsinic cid (DMA). In two soils the concentrtion of inorgnic As in rice grin ws decresed y 5e58%. The results demonstrte n effective stripping of ioville As from contminted pddy soils thus reducing As uptke y rice. Ó 211 Elsevier Ltd. All rights reserved. 1. Introduction Phytoremedition hs een suggested s n effective nd lowcost method to clen up contminted soils (Pilon-Smits, 25; Slt et l., 1998). However, so fr there re few successful exmples of its use to del with metl or metlloid contminted soils. This is due to numer of constrints including lck of rpidgrowing high-iomss hyperccumulting plnts, the concentrtions of metls/metlloids in soil eing too lrge, nd the presence of multiple contminnts often with low iovilility (McGrth nd Zho, 23; Zho nd McGrth, 29). Whilst removing the ulk of metls/metlloids from contminted soils is difficult tsk, it my e esier to strip the ioville frction of contminnts so s to decrese their trnsfer to the food chin (Hmon nd McLughlin, 23). An exmple is the use of Cd-ccumulting rice cultivrs to reduce ioville Cd in pddy soils nd susequent Cd uptke y rice (Murkmi et l., 29). Contmintion of rsenic (As) in pddy soils is widespred prolem due to irrigtion of As-lden groundwter in south nd southest Asi (Brmmer, 29), nd mining ctivities or pst uses of rsenicl grochemicls in other regions of the world (Willims et l., 27; Zhu et l., 28). Aneroic conditions in flooded Corresponding uthor. E-mil ddress: Fngjie.Zho@src.c.uk (F.-J. Zho). pddy soils re conducive to moiliztion of As leding to much enhnced As iovilility to rice plnts (Aro et l., 29; Li et l., 29; Willims et l., 27; Xu et l., 28). Rice is mjor source of inorgnic As for popultions sed on rice diet nd not exposed to high As in drinking wter (Kile et l., 27; Mehrg et l., 29). In ddition to concern over food sfety, ccumultion of As in pddy soil cn cuse phytotoxicity to rice plnts nd significnt reduction in grin yield, thus thretening the long-term sustinility of the rice cropping system in the ffected res (Khn et l., 21; Pnullh et l., 29). Vrious mitigtion methods hve een suggested to minimize As uptke y rice, including chnging pddy wter mngement, selection nd reeding of low As rice cultivrs, nd use of silicon fertilizers (Zho et l., 21). Phytoremedition is lso considered (Zho et l., 21), ut its effectiveness hs not een tested in the context of decresing As uptke y rice. Pteris vittt (Chinese rke fern) is well-known As hyperccumultor (M et l., 21). The plnt possesses n exceptionl ility to tke up, trnslocte nd tolerte As (Zho et l., 29). When grown in As-contminted soils, P. vittt ccumultes As in fronds often more thn 1 times the concentrtion in the soil (Cille et l., 24; Kertulis-Trtr et l., 26; Slido et l., 23; Shelmerdine et l., 29; Tu nd M, 22). In glsshouse pot experiments, P. vittt removed etween.1 nd 26% of the soil As, depending on soil As concentrtion nd iovilility, nd other soil fctors (Cille et l., 24; Shelmerdine et l., 29; Tu nd M, 22). In smll scle field tril, Kertulis-Trtr et l. (26) /$ e see front mtter Ó 211 Elsevier Ltd. All rights reserved. doi:1.116/j.envpol

2 374 W.-L. Ye et l. / Environmentl Pollution 159 (211) 3739e3743 reported tht the men concentrtion of soil As ws decresed from 19 to 14 mg kg 1 fter three hrvests of P. vittt; however, much of this pprent decrese ws likely due to smple vrition ssocited with high sptil heterogeneity of soil As, ecuse the totl uptke y the fern ccounted for only out 1% of the totl As in the surfce soil. The min limittions pper to e low iovilility of As in soil nd reltively low iomss production (Shelmerdine et l., 29). However, the iovilility limittion my ecome n dvntge if the im is to strip the ioville pool to enefit food sfety vi reduced As uptke y food crops. In the present study, we show tht phytoremedition with P. vittt mrkedly reduced As ccumultion in rice from five As-contminted pddy soils in pot experiments. 2. Mterils nd methods 2.1. Soils used Five pddy soils were used in this study, including 1 from West Bengl, Indi (), 2 from Bngldesh ( nd Sonrgon) nd 2 from Chin ( nd ). The sources of As contmintion were irrigtion of As-contminted groundwter (, nd Sonrgon), geogenic () nd mining (). The totl As concentrtion rnged from 7.6 to 74 mg kg 1 nd soil ph ws circum-neutrl to slightly lkline (Tle 1). Other soil properties re shown in Tle 1. Soils were collected from the plough lyer (e2 cm), ir-dried nd sieved through n 8 mm sieve Pot experiments Soils were plced in 1-L pots, ech contining.95 kg soil. Eight pots were prepred for ech soil; 4 were used for growing P. vittt nd the other 4 served s control (without P. vittt). For the pots used to grow P. vittt, sl fertilizers were mixed into the soils t 125 mg N kg 1 (NH 4 NO 3 ), 45 mg P kg 1 (KH 2 PO 4 ) nd 156 mg Kkg 1 (K 2 SO 4 nd KH 2 PO 4 ). P. vittt spores (originlly from the Oxford Botnic Grden) were germinted in generl-purpose compost (Petersfield Growing Mediums, Leicester, UK) nd pre-grown to the 3 frond stge. Two seedlings were trnsferred to ech pot. Soil moisture content ws mintined t ner the field cpcity level y dding deionized wter periodiclly s required during the growing period. The pots were rndomly rrnged on ench inside glsshouse (dy/night tempertures 28/25 c, light period 16 h per dy with nturl sunlight supplemented with sodium vpor lmps to mintin light intensity of >35 mmol m 2 s 1 ). Deionized wter ws dded dily s required. Plnts were grown for 9 months during which fully expnded fronds were collected in three hrvests. At the end of the experiment, rhizomes nd roots were lso collected. Plnt smples were wshed with deionized wter, nd dried t 65 C for 3 dys. Totl dry weights were recorded. The control pots were covered with lck plstic sheets to prevent weeds growing nd plced inside the sme glsshouse, with the soils eing mintined in ir-dry conditions. At the end of P. vittt growth, soils were ir-dried nd homogenized. Fifty grms of soil were collected from ech pot for nlysis. In the second experiment, soils from the control nd P. vittt tretment were repcked into 1-L pots (.8 kg per pot). Bsl fertilizers were dded (s in the first experiment). Deionized wter ws dded to mintin 2e3 cm depth of stnding wter. Fifteen dys lter, two pre-germinted rice seedlings (cv Itlic Crolin) were trnsplnted into ech pot. A rhizon smpler ws uried digonlly in the middle of the soil of ech pot for collecting soil pore wter t the rice flowering stge. Plnts were hrvested when they reched mturity (8 dys fter trnsplnting). Grins were seprted from strw nd dehusked. The weights of grin nd strw were recorded fter drying t 65 C for 3 dys Chemicl nlyses Soil orgnic cron ws determined y comustion method using LECO CNS nlyzer. Soil ph ws mesured with ph electrode in suspension of 1: soil:wter. Soil ville P ws determined y.5 M NHCO 3 extrction nd colorimetric mesurement (the Olsen method). Totl soil As concentrtions were determined y the digestion of finely ground soil (.1 g) using 5 ml of high-purity HNO 3 /HClO 4 (85/15 v/v) followed y nlysis using Inductively Coupled Plsm e Mss Spectrometry (ICP-MS) (Agilent, 75ce). Phosphte-extrctle As ws determined y extrction with.5 M (NH 4 H 2 PO 4 ) s descried previously (Song et l., 26), nd shown to reflect the potentil uptke y rice grown in different soils (Khn et l., 21). Finely ground plnt mterils (.2 g) were digested with high-purity HNO 3 /HClO 4 (87/13 v/v) nd As concentrtions in the digest solutions were determined y ICP-MS. A certified reference mteril (NIST 1568 rice flour) nd lnks were included for qulity ssurnce. Repeted nlysis of NIST 1568 (certified vlue.29.3 mg As kg 1 ) gve n excellent recovery of.29.2 mg As kg 1. Soil pore wter ws diluted with.1 M N 2 EDTA t 9:1 rtio to prevent Fe precipittion, filtered through sterilized.2 mm memrne filter, nd immeditely nlyzed for As specition using HPLC-ICP-MS (Agilent LC11 series nd Agilent ICP-MS 75ce) s descried previously (Xu et l., 28). The column used ws n nion-exchnge column (Hmilton PRP X1), nd the elunt contined 4.4 mm NH 4 H 2 PO 4, 4.4 mm NH 4 NO 3 nd.2 mm EDTA (ph 6.3) with flow rte of.7 ml min 1. For determintion of As specition in rown rice,.2 g powdered smples were weighed into microwve vessel nd extrcted with 1% HNO 3 in microwve digester (Sun et l., 28) Arsenic specition ws performed using HPLC-ICP-MS. The extrction method resulted in some oxidtion of rsenite to rsente; therefore, the sum of the two inorgnic As species ws presented together with methylted As species (Sun et l., 28). NIST 1568 rice flour ws included for qulity ssurnce. The sum of As species determined ws.3.1 mg As kg 1, compred with the certified totl As of.29.3 mg As kg 1. The percentges of As species were 34% inorgnic As nd 66% methylted As, similr to those reported in the literture (Heitkemper et l., 21; Sun et l., 28) Sttistics Dt were nlyzed y two-wy nlysis of vrince including soil nd phytoremedition s the fctors. Where necessry, dt were trnsformed logrithmiclly prior to ANOVA to stilize the vrince. Comprisons etween the mens of untreted nd P. vittt treted were mde using the lest significnt difference (LSD, P <.5). 3. Results 3.1. As uptke y Pteris vittt As concentrtion in fronds (weighted men of 3 cuttings) rnged from 45 to 26 mg kg 1 (Fig. 1). Frond As concentrtion ws the lowest in the soil with the lowest As concentrtion (), ut there were little differences mong the other four soils. The As ioconcentrtion fctor (the rtio of frond As concentrtion to soil totl As concentrtion) vried from 2.6 to 15.5, with the two Chinese pddy soils hving lower vlues thn the other three soils from the Bengl delt. When phosphte-extrctle As ws used s the denomintor, the ioconcentrtion fctor incresed to 3e76. Totl As uptke y P. vittt vried from.7 to 1.6 mg pot 1 (Fig. 1); most of the As ws in the fronds (men ¼ 9.3%). Totl As uptke ccounted for 1.4e12.7% (men ¼ 6.3%) of the totl As in the soils, nd 2.3e71.7% (men ¼ 42%) of the phosphte-extrctle As in the soil Effect of Pteris vittt on soil As concentrtion Compred with the control, soil totl As concentrtion decresed y 3.5e11.4% fter phytoremedition with P. vittt (Fig. 2). The decreses were generlly consistent with the mounts of As uptke Tle 1 Selected properties of soils used in the experiment. Soil smpling site Country Texture ph Orgnic C (%) Aville P (mg kg 1 ) Totl As (mg kg 1 ) Indi Lom Bngldesh Silt lom Sonrgon Bngldesh Silty cly lom Chin Cly Chin Cly Phosphte-extrctle As (mg kg 1 )

3 W.-L. Ye et l. / Environmentl Pollution 159 (211) 3739e As uptke (mg pot -1 ) y P. vittt. ANOVA showed tht the overll effect of P. vittt ws significnt (P ¼.2 sed on log-trnsformed dt); however, when LSD ws used to compre individul soils, no significnt differences etween untreted nd P. vittt treted soil were otined. In comprison, plnting of P. vittt decresed the phosphte-extrctle As to greter extent (11e38%) nd this effect ws highly significnt (P <.1) (Fig. 2). The decrese in the phosphte-extrctle As represented third to hlf of the totl uptke y P. vittt. There were no significnt differences in soil ph etween plnted nd unplnted tretments (dt not shown) Pv +Pv Sonrgon Fig. 1. The concentrtion of As in the fronds of Pteris vittt (men of three hrvests) () nd totl As uptke (). Dt re men þ SE. Sonrgon Fig. 2. The concentrtions of totl () nd phosphte-extrctle () As in untreted ( Pv) nd Pteris vittt treted (þpv) soils. Dt re men þ SE. indictes significnt (LSD, P <.5) difference etween the untreted nd treted soil Effects of Pteris vittt on As concentrtion nd specition in soil pore wter Soil pore wter ws collected during the rice flowering stge. Totl As concentrtions vried from 45 to 113 mg l 1 in the pore wter extrcted from the soils not plnted with P. vittt. Very high concentrtions (>1 mg l 1 ) were found in the two Bngldeshi pddy soils which hd history of irrigtion with As-contminted groundwter. After phytoremedition with P. vittt, As concentrtions in soil pore wter decresed y 18e77% (P <.1), with the decrese eing most pronounced in the two Bngldeshi soils (Fig. 3). Arsenite ws the predominnt species in the soil pore wter, ccounting for 77e96% of the totl As, nd the reminder ws rsente. Phytoremedition with P. vittt significntly (P <.1) decresed the percentge of rsenite in soil pore wter from 93% to 86%, verged cross ll soils As uptke nd specition in rice The growth of rice plnts ppered to e norml in oth untreted nd P. vittt treted soils. However, grin iomss ws significntly lower in three soils (Sonrgon, nd ) fter phytoremedition compred with untreted soils (Supporting informtion, Figure S1). Strw iomss ws lso significntly lower in one soil () fter phytoremedition. At mturity, the As concentrtions in rice grin, husk nd strw grown in the P. vittt treted soils were significntly (P <.1) lower thn those grown in the untreted soils (Fig. 4). The decrese vried from 18 to 83% for grin As, from 24 to 91% for husk As nd from 42 to 78% for strw As. In the four pddy soils with totl As >1 mg kg 1, grin As concentrtion ws more thn hlved (6e83% decrese) fter phytoremedition with P. vittt. Phytoremedition lso produced mrked effect on specition of As in rice grin y decresing the concentrtion of DMA (dimethylrsinic cid) more thn tht of inorgnic As (Fig. 5). DMA ws the predominnt As species (73e78%) in the grin smples produced from the untreted soils, except the low As soil which produced grin with only 21% DMA. After phytoremedition, DMA ws not detectle in the grin smples produced from three soils (, nd ) nd ecme minor component (21e31%) of totl As in the other two Bngldeshi soils ( nd Sonrgon). Phytoremedition decresed the concentrtion of inorgnic As in rice grin significntly only in the two Chinese soils (58 nd 5% decrese in nd, respectively). 4. Discussion The present study hs demonstrted tht phytoremedition with P. vittt cn mrkedly reduce As ccumultion in rice (Fig. 4). As concentrtion (µg l -1 ) As(V) As(III) -Pv +Pv -Pv +Pv -Pv +Pv -Pv +Pv -Pv +Pv Sonrgon Fig. 3. The concentrtions of rsente (As(V)) nd rsenite (As(III)) in soil pore wter extrcted from untreted ( Pv) nd Pteris vittt treted (þpv) soils during rice flowering stge. Dt re men SE. indictes significnt (LSD, P <.5) difference in totl solule As etween the untreted nd treted soil.

4 3742 W.-L. Ye et l. / Environmentl Pollution 159 (211) 3739e3743 As concentrtion (µg g -1 ) As concentrtion ( µ g g -1 ) As concentrtion ( µ g g -1 ) c -Pv +Pv Sonrgon The mgnitude of decrese ws remrkle especilly in the four most contminted pddy soils (6e83% decrese). Totl As removl from the soils y P. vittt ws reltively smll compred with the totl mount of As in the soils (only 3.5e11.4%), which is comprle to the rnge of.1e13% reported for 21 historiclly contminted soils in glsshouse experiment y Shelmerdine et l. (29). The decrese in the potentilly ioville pool ws greter: 11e38% in phosphte-extrctle As nd 18e77% in soil pore wter As (Figs. 2 nd 3). These results suggest tht P. vittt ws effective t stripping ioville As from the soil, nd it is this ility tht led to lrge decreses in As ccumultion y rice. The Fig. 4. The concentrtions of As in grin (), husk () nd strw (c) of rice in untreted ( Pv) nd Pteris vittt treted (þpv) soils. Dt re men þ SE. indictes significnt (LSD, P <.5) difference etween the untreted nd treted soil. As concentrtion (µg g -1 ) DMA Inorgnic As -Pv +Pv -Pv +Pv -Pv +Pv -Pv +Pv -Pv +Pv Sonrgon Fig. 5. Arsenic specition in rice grin in untreted ( Pv) nd Pteris vittt treted (þpv) soil. Dt re men SE. indictes significnt (LSD, P <.5) difference in the sum of ll As species etween the untreted nd treted soil. ility of As uptke y P. vittt is lso pprent when compred with tht of rice with the mount of As tken up y the hyperccumultor eing 11e176 times greter thn rice. It is interesting tht phytoremedition with P. vittt lso impcted on As specition in rice grin (Fig. 5). DMA ws the dominnt form in the grin produced from 4 of the untreted soils ut ecme minor species or undetectle fter phytoremedition. The high DMA% in the grin from untreted soils could e ttriuted to the wy the rice plnts were grown in the pot experiment with continuous flooding over the entire growth period. It hs een shown tht continuous flooding led to higher grin As concentrtion s well s higher DMA% (Aro et l., 29; Li et l., 29; Xu et l., 28). A comprison of field versus pot grown rice using the sme rice cultivr nd two of the sme soils ( nd Sonrgon, s used in the present study) showed higher DMA% in the ltter, proly ecuse the ltter ws mintined under flooded conditions throughout the entire growth period (Khn et l., 21). The effect of growing P. vittt on decresing rice grin DMA my e explined y much decresed inorgnic As concentrtion in the soil pore wter (Fig. 3), which my susequently decrese As methyltion y soil microes. No methylted As species were detected in the soil pore wter smples; however, this my e ecuse of the wy soil pore wter ws preserved with the ddition of EDTA in the present experiment. Our recent studies showed tht DMA ecme detectle in soil pore wter preserved with HCl cidifiction (unpulished). It is often ssumed tht methylted As is less toxic to humns thn inorgnic As (Schoof et l., 1999), lthough there is lck of toxicologicl dt for methylted As species. Methylted As in the pentvlent form cn e reduced to trivlent oxidtion stte nd trivlent methylted As species re extremely toxic (Stylo et l., 2). Therefore, DMA in rice grin my not e considered s hrmless. Phytoremedition decresed the concentrtion of inorgnic As in rice grin y >5% in the two Chinese soils; this effect ws not significnt in the other three soils due to unknown resons. Phytoremedition with P. vittt resulted in smller rice iomss in some of the soils tested (Supporting informtion, Figure S1). This ws unexpected ecuse decresed As concentrtions in soil pore wter should hve llevited As toxicity to rice, lthough in fct no overt toxicity symptoms were oserved in the plnts grown in the untreted soils. Possile resons for the negtive effect re depletion of nutrients or growth-inhiiting root exudtes or decomposition products of P. vittt roots. These remin to e investigted in the future. Although the present study hs demonstrted lrge effect of phytoremedition on decresing As uptke y rice, it should e orne in mind tht the experiment ws performed in pots under glsshouse conditions. Field trils re needed to confirm if phytoremedition cn e similrly effective under locl rice growing conditions. Another issue to consider is whether the effect is long lsting ecuse of the possiility of re-distriution of As to the ioville pool following phytoremedition. A further constrint is whether frmers cn fford to set side their lnd for phytoremedition. Nevertheless, this study hs proved the concept of using n As hyperccumultor plnt to strip ioville As from soil to reduce its trnsfer to the food chin. Acknowledgements Rothmsted Reserch is n institute of the Biotechnology nd Biologicl Sciences Reserch Council. M. A. Khn received funding from the Rothmsted Interntionl Fellowship scheme. We thnk Professors Rfique Islm, Yonggun Zhu nd Tpsh Dsgupt for providing the soils used in this study.

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