Effect of selenium in soil on the toxicity and uptake of arsenic in rice plant

Chemosphere 239 (2020) 124712

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Effect of selenium in soil on the toxicity and uptake of arsenic in rice plant Ganga Raj Pokhrel a, 1, Kai Teng Wang a, 1, HongMao Zhuang a, 1, YongChen Wu a, Wei Chen a, Yan Lan a, Xi Zhu a, Zhong Li a, FengFu Fu b, **, GuiDi Yang a, * a

Fujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, 350002, China Key Laboratory for Analytical Science of Food Safety and Biology of Ministry of Education, Fujian Provincial Key Lab of Analysis and Detection for Food Safety, College of Chemistry, Fuzhou University, Fuzhou, Fujian, 350116, China

b

h i g h l i g h t s
Selenite and selenate are found to facilitate the arsenate adsorption by paddy soil.
Selenite and selenate inhibited the uptake of arsenate by rice roots.
Antagonism between Se and As depended on rice cultivar, As species and concentration.
Selenate has stronger inhibition on inorganic arsenic transfer factors than selenite.
Selenium has synergistic and inhibiting effects on TMAO(V) and DMA(V).

a r t i c l e i n f o

a b s t r a c t

Article history: Received 31 January 2019 Received in revised form 27 August 2019 Accepted 29 August 2019 Available online 30 August 2019

Selenium can regulate arsenic toxicity by strengthening antioxidant potential, but the antagonism between selenite or selenate nutrient and the translocation of arsenic species from paddy soil to different rice organs are poorly understood. In this study, a pot experiment was designed to investigate the effect of selenite or selenate on arsenite or arsenate toxicity to two indica rice cultivars (namely Ming Hui 63 and Lu You Ming Zhan), and the uptake and transportation of arsenic species from paddy soil to different rice organs. The results showed that selenite or selenate could significantly decrease the arsenate concentration in pore water of soils, and thus inhibited arsenate uptake by rice roots. However, the existence of selenite or selenate didn't decrease arsenate concentration in rhizosphere pore water of two indica rice cultivars. There existed good antagonistic effect between selenite or selenate and the uptake of arsenite and arsenate in rice plant in the case of low arsenic paddy soil. However, this antagonism depended on rice cultivars, arsenic species and arsenic level in soil. There existed both synergistic and inhibiting effects between the addition of selenite or selenate and the uptake of trimethylarsinoxide and dimethylarsinic acid by two indica rice cultivars, but the mechanism was unclear. Both selenite and selenate are all effective to decrease the translocation of inorganic arsenic from the roots to their aboveground rice organs in arsenite/arsenate-spiked paddy soil, but selenate had stronger inhibiting effect on their transfer factors than selenite. © 2019 Elsevier Ltd. All rights reserved.

Handling Editor: X. Cao Keywords: Arsenic Rice (Oryza sativa L.) Selenium Heavy metallic ion Toxicity Transportation

1. Introduction Rice grain is the staple food for the majority of the population in

* Corresponding author. ** Corresponding author. E-mail addresses: [email protected] (F. Fu), [email protected] (G. Yang). 1 These authors contributed equally to this work. https://doi.org/10.1016/j.chemosphere.2019.124712 0045-6535/© 2019 Elsevier Ltd. All rights reserved.

the world, but its accumulation of toxic arsenic (As) species makes it become one of the major sources of As intake by human beings (Rahman et al., 2008; Li et al., 2011). Arsenic is a non-essential and toxic element, and it can hinder the growth of rice plant and inhibit rice's photosynthesis and yield (Abdein and Meharg, 2002; Yang et al., 2015; Duncan et al., 2017). Geogenic source, mining activities, rainwater leaching and waste discharge from various industrial and agricultural activities into the environment led to the

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increase of As amount into the paddy soil and ground water (Senesil et al., 1999; Shaheen et al., 2017), moreover, rice is highly efficient to accumulate the inorganic As in flooded soil (Abedin et al., 2002). Thus, the rising As concentration in pore water of soils eventually increased its uptake by rice plant and its accumulation in rice grain, which might pose a serious risk on human health (Zhu et al., 2008a, 2008b). Therefore, it is essential to decrease the As toxicity on rice growth and its transportation from paddy soil to rice grain (Saifullah et al., 2018). There is no evidence that selenium (Se) is an essential element to plant, but it is an essential micronutrient for humans and animals (Fordyce, 2013). Various studies showed that Se could alleviate heavy metal stress on plant growth and enhance plant antioxidant capacity (Malik et al., 2012; Lin et al., 2012; Han et al., 2015), the addition of Se into hydroponic solution significantly decreased As toxicity to rice seedling (Kumar et al., 2016; Chauhan et al., 2017). Inorganic species of As and Se elements, namely arsenite [As(III)], arsenite [As(V)], selenite [Se(IV)] and selenite [Se(VI)], are the major forms present in flooded soil (Elrashidi et al., 1987; Zheng et al., 2013), their close position in the periodic table makes them show similar characteristics in their uptake and transportation from soil to plants. It was reported that As(III) was transported into plant roots by silicon transporters (Ma et al., 2008; Tripathi et al., 2013) and As(V) is mediated by phosphate transporters (Mehrag and Macnair, 1992; Meharg and Hartley-Whitaker, 2002). It was also reported that Se(IV) was transported into plant roots by both silicon transporters and phosphate transporters (Zhao et al., 2010; Zhang et al., 2014), Se (VI) was transported into plant roots by sulfate transporters and might be inhibited by phosphate (Hawkesford and Zhao, 2007; Li et al., 2008). Thus, the antagonism might exist between inorganic As and inorganic Se uptake by rice roots. In earlier reports about their antagonism effect, most researches focused on short-term hydroponic experiments, some studies verified that the addition of Se(IV) or Se(VI) decreased the accumulation of total As concentration in rice roots or shoots (Kumar et al., 2016; Kaur et al., 2017; Camara et al., 2018), while some studies reported that the addition of Se(IV) or Se(VI) improved the uptake of inorganic As, namely As(III) and As(V), by rice roots, moreover, Se(IV) have stronger interaction with As(III) than As(V) (Hu et al., 2014). Till the date, there was no agreed conclusion about the competitive uptake and transportation between inorganic As and inorganic Se in short-term hydroponic solution. Wan et al. (2018) reported from a pot experiment that Se(IV) addition decreased total As concentration in rhizosphere pore water of rice plants, while increased total As concentration in rice grain under flooded condition, but the competitive uptake and transportation from paddy soil to rice grain between inorganic As and inorganic Se was also poorly understood. In this study, two indica rice cultivars, namely Ming Hui 63 (MH63) and Lu You Ming Zhan (LYMZ), were used as the materials and a pot experiment was designed to investigate the effect of inorganic Se [Se(IV) and Se(VI)] regulation on inorganic As [As(III) or As(V)] toxicity to different rice cultivars, and the uptake and transportation of As species from paddy soil to different rice grain. On the other hand, the effect of inorganic Se regulation on As species in flooded soil without rice plants was also investigated to further obtain the effect of rice cultivars on the As species in flooded soil.

of China, during rice growth period of June to October 2017. The day and night temperature was at the range of 25e37  C, the humidity was at the range of 68e90%, and day length was about 13 h. Two indica rice cultivars (MH63 and LYMZ) were used in this study, from the Rice Research Institute, Academy of Agriculture Sciences, Fujian of China. Rice cultivars were planted in plastic buckets (0.26 m height with 0.30 m top and 0.23 m bottom diameter, respectively). Four rice seedlings were planted per pot and one pot represented one replication. Silty loam soil was used with available N 37.83 ± 1.11 mg/kg, available P 21.92 ± 1.89 mg/kg, available K 54.89 ± 0.56 mg/kg, total As 3.63 ± 0.21 mg/kg and pH 6.88 ± 0.02. The total Se concentration in soil was lower than detection limit of Inductively Coupled Plasma-Mass Spectrometry (ICP-MS). Fertilizer application and cultivation management throughout their growing period until maturing were based on the description of our lab (Li et al., 2018). 2.2. Arsenic and selenium treatments The rice seedling of cultivar MH63 and LYMZ (at the 4-leaf stage) was transferred into sandy loam soil (4 seedlings each pot) as described in Materials and methods 2.1 and grown in pot soil (12 kg soil per pot) within nine different treatments (4 replications each), respectively. Treatment 1 (CT00), no As or Se was spiked into the soil; Treatment 2 (CT04), 4.00 mg Se(IV) was spiked into per kg soil; Treatment 3 (CT06), 4.00 mg Se(VI) was spiked into per kg soil; Treatment 4 (AT30), 50.00 mg As(III) was spiked into per kg soil; Treatment 5 (AT34), 50.00 mg As(III) and 4.00 mg Se(IV) were spiked into per kg soil; Treatment 6 (AT36), 50.00 mg As(III) and 4.00 mg Se(VI) were spiked into per kg soil; Treatment 7 (AT50), 50.00 mg As(V) was spiked into per kg soil; Treatment 8 (AT54), 50.00 mg As(V) and 4.00 mg Se(IV) were spiked into per kg soil; Treatment 9 (AT56), 50.00 mg As(V) and 4.00 mg Se(VI) were spiked into per kg soil. For all treatments, As(III), As(V), Se(IV) and Se(VI) were added into paddy soil as NaAsO2, Na2HAsO4∙7H2O, H2SeO3 and H2SeO4, respectively. 50.00 mg As(III) or As(V) and 4.00 mg Se(IV) or Se(VI) in per kg soil meant the concentration of element As and Se. The treatment solutions with As(III), As(V), Se(IV) or Se(VI) were adjusted to pH5.50 and mixed with paddy soil in plastic buckets and stirred thoroughly to make homogeneity before the rice seedling of cultivar MH63 and LYMZ was transplanted. 2.3. Collection of rhizosphere pore water and pore water of soils sample About 40.00 mL of rhizosphere pore water was collected from the rooting zone using 10.00 cm capillary sampler (Rhizon, Shanghai kangwen biotechnology co. LTD) at tillering stage, booting stage, grouting stage and maturing stage of cultivars MH63 and LYMZ, respectively. Similarly, about 40.00 mL of pore water of soils was also collected from the central zone of plastic buckets using 10.00 cm capillary sampler at the corresponding stages without rice plants. Then the collected water sample was filtered through 0.22 mm polypropylene membranes, kept in 20  C until further determination of pH, oxidation-reduction potential (ORP or Eh), total organic carbon (TOC), total carbon (TC), inorganic carbon(IC), total nitrogen (TN), and As species by Ion Chromatography (IC)-ICPMS as described in Section 2.6.

2. Materials and methods 2.4. Soil properties and plant physiological measurement 2.1. Plant materials and growth conditions Pot cultivation was carried out in the experimental field of Fujian Agriculture and Forestry University, Fuzhou, Fujian province

The pH value and Eh value in rhizosphere pore water were measured using pHS-3C meter, the concentration of TC, IC and TN contained in rhizosphere pore water samples were determined

G.R. Pokhrel et al. / Chemosphere 239 (2020) 124712

using total organic carbon analyzer (TOC-L, Shimadzu, Tokyo, Japan), the concentration of TOC was obtained by difference value of TC and IC. Plant height was measured using a ruler with the precision of 0.01 cm at tillering, booting, grouting and maturing stages, the chlorophyll SPAD value in the fresh rice leaves was determined by a SPAD-502 Plus chlorophyll meter at the same stages. Each pot contained four rice plants and the average of each physiological parameter was considered as one replication. Rice cultivars were harvested after maturation of the grain (grains color was sunset yellow), the average number of matured panicles per rice plant were counted. Rice plants were taken out from the PVC pot with its roots. Soil and sandy materials were removed using tap water. Then rice plants were thoroughly washed with tap water and Milli-Q water till there were no any coarse particles adsorbed on the rice plants. Rice organs, such as roots, stems, sheaths, leaves and grains, were separated by ceramic scissors, and dried at 50  C for 48 h until constant weight, their dried weight and rice yield were recorded. At the same time, some fresh rice organs of other plants within each replication, including roots, stems, sheaths and leaves, were blotted dry, crushed into fine powder by tissuelyser-24 and stored at 20  C in separate plastic bags for the extraction of As species. Grains were air dried at room temperature (~25  C). Grains were dehulled in a motorized dehusker and separated into whole kernel and bran. Whole kernel and bran were grind to fine powder by tissuelyser-24 and stored in desiccator for the analysis of As species.

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detected by IC-ICP-MS under optimal conditions shown in Supplementary Table S1 (see Supplementary information, SI). The rice samples spiked with trimethylarsinoxide [TMAO(V)], dimethylarsinic acid [DMA(V)], As(III), monomethylarsonic acid [MMA(V)] and As(V) were also detected with the same manner to obtain recovery. 2.6. Analysis of arsenic species Arsenic speciation in rhizosphere pore water, pore water of soils and the extract of roots, stems, sheaths, leaves, kernel and bran, was determined using IC-ICP-MS (IC, Dionex ICS-1100, Thermofisher, USA; ICP-MS, NexION 300X, PerkinElmer, USA). Arsenic species [TMAO(V), DMA(V), As(III), MMA(V) and As(V)] were separated using an anion-exchange column (IonPac AS23, 4  250 mm, 10 mm). The mobile phase contained 10.00 mM Diammonium hydrogen phosphate [(NH4)2HPO4] and 8.00 mM ammonium nitrate [NH4NO3] (pH 10.0, adjusted by NH4OH), which was pumped through the column at 1.00 mL min1. The outlet of the separation column was connected to the ICP-MS. The qualitative and quantitative analysis of TMAO(V), DMA(V), As(III), MMA(V) and As(V) in rhizosphere pore water, pore water of soils and the extract of different organs of rice plants was similar to our previous reports (Shuai et al., 2016; Li et al., 2017). Arsenic species in rhizosphere pore water and pore water of soils was measured within one week after sampling, As species in the extract of rice organs was measured within 24 h after extraction.

2.5. Extraction of arsenic species 2.7. Data analysis About 0.1 g crushed samples (with the precision of 0.00001 g) were weighed into 100 mL polyteterfluoroethylene (PTFE) microwave tube and added with 10.00 mL of 1.00% (v/v) nitric acid. The Microwave vessels were capped and placed in the rotor of an ETHOS UP microwave extraction apparatus (Milestone High Performance Microwave Digestion Technology, Italy) according to our previous report (Qiu et al., 2018). The operating program of the system was implemented as 120  C for 25 min (5 min ramp time) and dropped to 60  C within 5 min. After the extraction was

The total concentration of each As species in roots, stems, sheaths and leaves of cultivars MH63 and LYMZ was calculated on a fresh weight (FW) basis, while their total concentration in bran and kernel was calculated on a dried weight (DW) basis. The total concentration of each arsenic species in rice plant, the total content of inorganic arsenic (iAs) and the transfer factor (TF) of iAs were calculated as follows:


CTMAOðVÞAs ¼ CTMAOðVÞAs  RootFW þ CStemTMAOAs  StemFW þ CsheathTMAOAs  SheathFW þ . RootFW CLeafTMAOAs  LeafFW þ CBranTMAOAs  BranDW þ CKernelTMAOAs  KernelDW CDMAðVÞAs ¼ ðCRootDMAAs  RootFW þ CStemDMAAs  StemFW þ CsheathDMAAs  SheathFW þ . RootFW CLeafDMAAs  LeafFW þ CBranDMAAs  BranDW þ CKernelDMAAs  KernelDW
CAsðIIIÞAs ¼ CRootAsðIIIÞAs  RootFW þ CStemAsðIIIÞAs  StemFW þ CsheathAsðIIIÞAs  SheathFW þ . CLeafAsðIIIÞAs  LeafFW þ CBranAsðIIIÞAs  BranDW þ CKernelAsðIIIÞAs  KernelDW RootFW
CAsðVÞAs ¼ CRootAsðVÞAs  RootFW þ CStemAsðVÞAs  StemFW þ CsheathAsðVÞAs  SheathFW þ . CLeafAsðVÞAs  LeafFW þ CBranAsðVÞAs  BranDW þ CKernelAsðVÞAs  KernelDW RootFW

finished, the extract was diluted to constant volume with Milli-Q water, centrifuged (12000 rotation per min, 3 min) and filtered through 0.22 mm polypropylene membranes into polyethylene centrifuge tubes for the analysis of As species. Then, the concentrations of different As species in the extract were separated and


TRootiAs ¼ CRootAsðIIIÞAs þ CRootAsðVÞAs  RootFW

(1)

(2)

(3)

(4)

(5)

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TStemiAs ¼ CStemAsðIIIÞAs þ CStemAsðVÞAs  StemFW

(6)


TSheathiAs ¼ CSheathAsðIIIÞAs þ CSheathAsðVÞAs  SheathFW (7) 
TLeafiAs ¼ CLeafAsðIIIÞAs þ CLeafAsðVÞAs  LeafFW

(8)


TBraniAs ¼ CBranAsðIIIÞAs þ CBranAsðVÞAs  BranDW

(9)


TKerneliAs ¼ CKernelAsðIIIÞAs þ CKernelAsðVÞAs  KernelDW (10) TFstem to root ¼ TstemiAs =TRootiAs

(11)

TFsheath to root ¼ TsheathiAs =TRootiAs

(12)

. ¼ TLeafiAs TRootiAs

(13)

TFBran to root ¼ TBraniAs =TRootiAs

(14)

TFKernel to root ¼ TKerneliAs =TRootiAs

(15)

TFLeaf

to root

2.8. Statistical analysis Each sampling was conducted in 4 biological replications and their average values were used for statistical analysis. Software DPS7.5 was used to conduct the significant test by least significant difference (LSD) among different treatments. 3. Results and discussion

species (Fig. 1B). The addition of Se(IV) or Se(VI) in soils significantly decreased the concentration of As(III) and As(V) in pore water of soils, and facilitated the oxidation of As(III) and the adsorption of As(V) by paddy soil. In rhizosphere pore water of As(III)/As(V)-spiked soils planting cultivar MH63, As(III) percentage was continuously increased from tillering stage to maturation stage and reached the highest at maturation stage, which accounted for 78.58%e92.12% of the sum concentration of As species. The addition of Se(VI) more notably decreased the As(III) concentration in As(V)-spiked rhizosphere pore water of cultivar MH63, in comparison with Se(IV) (Fig. 1B). Arsenite percentage in As(III)/As(V)-spiked rhizosphere pore water of cultivar LYMZ was also increased from tillering stage to maturation stage, but reached the highest at its booting stage, which accounted for 66.67%e88.04% of the sum concentration of As species. The addition of Se(IV) decreased the As(III) concentration in As(V)-spiked rhizosphere pore water of cultivar LYMZ more notably, in comparison with Se(VI) (Fig. 1B). Above results indicated that the antagonism between Se(IV)/Se(VI) and As(III) depended on rice cultivars. Arsenite concentration in rhizosphere pore water of cultivars MH63 and LYMZ was much higher than that in pore water without rice planting, which suggested that As(III) in rhizosphere pore water of cultivars MH63 and LYMZ mainly originate from the secretion of their roots (Xu et al., 2007). Moreover, the As(III) concentration in rhizosphere pore water of cultivar LYMZ was much higher than that of cultivar MH63, which might be brought by stronger secretion of cultivar LYMZ roots for As(III) or quicker oxidation of cultivar MH63 roots for As(III). Although the addition of Se(IV) and Se(VI) decreased the concentration of As(V) in pore water of As(III)/As(V)-spiked soils without rice planting (Fig. 1B). However, the addition of Se(IV) and Se(VI) didn't decrease the As(V) concentration in rhizosphere pore water of cultivar MH63 or LYMZ. It was reported that arsenate was taken up by rice roots through phosphate transporters (Meharg and Hartley-Whitaker, 2002). Inside the roots tissue, As(V) could be further reduced into more poisonous As(III) and excreted out of the roots. The above concentration relationship between As(III)/As(V) and Se(IV)/Se(VI) showed that Se(IV) and Se(VI) could inhibit the As(V) uptake of rice roots and had obvious antagonism on the As(V) uptake of rice roots.

3.1. Effect of selenium on arsenic species in rhizosphere pore water Four As species, namely TMAO(V), DMA(V), As(III) and As(V), were detected in both rhizosphere pore water and pore water of soils, in despite of rice plant was planted or not. But, their change in percentage and concentration was significantly different (Fig. 1). In comparison with Se(IV), the addition of Se(VI) in soil more obviously decreased the concentration of TMAO(V) and DMA(V) in rhizosphere pore water in the case of low arsenic paddy soil (Fig. 1A). It is generally recognized that TMAO(V) and DMA(V) in pore water are from the methylation of inorganic As species by microorganisms in the paddy soil (Qin et al., 2006; Lomax et al., 2011). However, the concentration of TMAO(V) and DMA(V) in rhizosphere pore water of cultivars MH63 and LYMZ was much higher than that without rice planting, indicating that oxygen secretion from rice plants accelerated the methylation of inorganic As species by microorganisms in the paddy soil. For the same As(III)/As(V)-spiked soils, the concentration of TMAO(V) and DMA(V) in rhizosphere pore water of cultivar LYMZ was higher than that of cultivar MH63 (Fig. 1B), indicating that cultivar LYMZ had stronger respiration than cultivar MH63 in As(III)/As(V)-spiked soil. In pore water of As(III)/As(V)-spiked soils (without rice plants), As(V) was found to be the predominant As species, which accounted for 52.96%e94.97% of the sum concentration of As

3.2. Effect of selenium regulation on pH, Eh, TOC, TC, IC and TN in rhizosphere pore water under arsenite or arsenate stress or not Whether As(III)/As(V) was spiked into soil or not, the addition of Se(IV) or Se(VI) decreased the pH and Eh value of rhizosphere pore water of cultivar MH63 from tillering stage to maturation stage, moreover, the addition of Se(VI) had greater effect on the pH and Eh value of rhizosphere pore water in cultivar MH63 than the addition of Se(IV). The similar results were also observed in pore water of soils without rice planting, but the results for cultivar LYMZ are different (Fig. S1 and Fig. S2 in SI). The Eh and pH value could affect As species existing in rhizosphere pore water and pore water of soils (Masscheleyn et al., 1991), the higher Eh and pH value in rhizosphere pore water of cultivar LYMZ after filling stage led to lower As(III) percentage in rhizosphere pore water of cultivar LYMZ, compared with cultivar MH63 (Fig. 1). The TN concentrations in rhizosphere pore water of cultivars MH63 and LYMZ were much lower than that of pore water without rice planting (Fig. S3 in SI), indicating that the microbial activity in rhizosphere pore water of cultivars MH63 and LYMZ was better than that without rice plants. Increasing concentrations of TOC, TC and IC from tilling stage to booting stage of two rice cultivars further verified that rice roots facilitated the microbial respiration. Therefore, the concentrations of organic As species such as

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TMAO(V) and DMA(V) in rhizosphere pore water of cultivars MH63 and LYMZ were much higher than that without rice plants. Thus, the toxicity of inorganic As on the growth of rice plants was decreased because of this kind of methylation, so this is also one kind of self-detoxification mechanism from the rice system. 3.3. Effect of selenium regulation on the accumulation of arsenic species in rice organs 3.3.1. Effect of selenium regulation on arsenic species uptake in rice organs of cultivar MH63 At maturing stage, whether As(III)/As(V) was spiked into paddy soil or not, only As(III) and As(V) were detected in the roots, stems, sheaths and leaves of cultivar MH63, and only DMA(V) and As(III) were detected in the kernel of cultivar MH63. However, DMA(V), As(III) and As(V) were detected in the bran of cultivar MH63 (Fig. 2). In low arsenic paddy soil, the addition of Se(IV) significantly (p < 0.01) decreased the As(III) concentration in the roots, stems, sheaths, leaves, bran and kernel of cultivar MH63 by (100.00 ± 0.00)%, (68.37 ± 2.65)%, (49.33 ± 2.07)%, (38.80 ± 1.96)%, (37.04 ± 1.92)% and (28.18 ± 1.43)% respectively, and also significantly (p < 0.01) decreased the As(V) concentration in the roots, sheaths, leaves and bran of cultivar MH63 by (59.98 ± 1.87)%, (34.66 ± 1.75)%, (36.77 ± 1.94)% and (67.36 ± 2.89)% respectively relative to the standalone low arsenic soil (Fig. 2A). The addition of Se(VI) significantly (p < 0.01) decreased the As(III) concentration in the roots, stems, sheaths, leaves, bran and kernel of cultivar MH63 by (100.00 ± 0.00)%, (77.96 ± 3.02)%, (47.97 ± 2.04)%, (52.87 ± 2.01)%, (47.72 ± 2.5)% and (100.00 ± 0.00)% respectively, and also decreased the As(V) concentration in the roots, stems, sheaths, leaves and bran of cultivar MH63 by (4.37 ± 0.34)%, (27.55 ± 1.23)%, (54.56 ± 2.38)%, (100.00 ± 0.00)% and (65.43 ± 2.83)% respectively relative to the standalone low arsenic soil (Fig. 2A). There existed good antagonistic effects between the addition of Se(IV)/Se(VI) and the As(III)/As(V) uptake by cultivar MH63. Moreover, the Se(VI) addition had better inhibiting effect on the uptake of As(III) and As(V) by cultivar MH63 than the Se(IV) addition (Fig. 2A). In As(III)-spiked paddy soil, the addition of Se(IV) decreased the As(III) concentration in the roots, stems and kernel of cultivar MH63 by (100.00 ± 0.00)%, (9.42 ± 0.56)%% and (36.09 ± 1.84)% respectively, and also decreased the As(V) concentration in the roots, sheaths, leaves and bran of cultivar MH63 by (46.53 ± 1.78)%, (10.79 ± 0.48)%, (34.22 ± 1.65)% and (29.18 ± 1.32)% respectively relative to the standalone As(III)-spiked treatment (Fig. 2B). The addition of Se(VI) significantly (p < 0.01) decreased the As(III) concentration in the roots, stems and kernel of cultivar MH63 by (100.00 ± 0.00)%, (20.01 ± 0.96)% and (25.18 ± 1.32)% respectively, and also significantly (p < 0.01) decreased the As(V) concentration in the roots, leaves and bran of cultivar MH63 by (24.26 ± 1.13)%, (34.78 ± 1.63)% and (29.00 ± 1.45)% respectively relative to the standalone As(III)-spiked treatment (Fig. 2B). Different from low arsenic paddy soil, the Se(VI) addition had better inhibiting effect on As(III) uptake, while Se(IV) addition had better inhibiting effect on As(V) uptake by cultivar MH63 relative to the standalone As(III)spiked treatment by cultivar MH63 (Fig. 2B). In As(V)-spiked paddy soil, the addition of Se(IV) significantly (p < 0.01) decreased the As(III) concentration in the roots, stems and leaves of cultivar MH63 by (100.00 ± 0.00)%, (22.11 ± 1.23)%

and (16.29 ± 1.05)% respectively, and also significantly (p < 0.01) decreased the As(V) concentration in the stems of cultivar MH63 by (47.63 ± 2.01)% relative to the standalone As(V)-spiked treatment (Fig. 2B). The addition of Se(VI) decreased the As(III) concentration in the roots, stems, sheaths, leaves, bran and kernel of cultivar MH63 by (100.00 ± 0.00)%, (60.02 ± 2.16)%, (37.08 ± 1.53)%, (56.78 ± 2.23)%, (63.97 ± 2.39)% and (4.76 ± 0.32)% respectively, and also decreased the concentration of As(V) in the roots, stems, sheaths and bran of cultivar MH63 by (12.74 ± 0.78)%, (50.41 ± 2.38)%, (2.27 ± 0.24)% and (18.36 ± 1.01)% respectively relative to the standalone As(V)-spiked treatment (Fig. 2B). Similar to low arsenic paddy soil, Se(VI) addition had better inhibiting effect on the uptake of As(III) and As(V) by cultivar MH63 than Se(IV) addition (Fig. 2B). 3.3.2. Effect of selenium regulation on arsenic species uptake in rice organs of cultivar LYMZ At maturing stage, whether As(III)/As(V) was spiked into paddy soil or not, there also detected only As(III) and As(V) in the roots of cultivar LYMZ, DMA(V) and As(III) in the kernels of cultivar LYMZ, TMAO(V), As(III) and As(V) in the stems of cultivar LYMZ. However, four As species, namely TMAO(V), DMA(V), As(III) and As(V), were detected in the sheaths, leaves and bran of cultivar LYMZ (Fig. 2). In low arsenic paddy soil, the addition of Se(IV) significantly (p < 0.01) decreased the As(III) concentration in the roots, stems and bran of cultivar LYMZ by (41.98 ± 2.27)%, (29.47 ± 1.06)% and (27.33 ± 1.12)% respectively, and also decreased the As(V) concentration in the stems, leaves and bran of cultivar LYMZ by (38.01 ± 1.98)%, (15.99 ± 1.03)% and (4.18 ± 0.32)% respectively (Fig. 2A). The addition of Se(VI) significantly (p < 0.01) decreased the As(III) concentration in the stems, sheaths, leaves, bran and kernel of cultivar LYMZ by (57.32 ± 2.35)%, (45.67 ± 1.68)%, (59.18 ± 2.06)%, (70.96 ± 2.66)% and (41.67 ± 1.34)%, and also significantly (p < 0.01) decreased the As(V) concentration in the stems, sheaths, leaves and bran of cultivar LYMZ by (57.20 ± 2.43)%, (41.60 ± 1.48)%, (27.41 ± 1.83)% and (57.17 ± 2.85)%, respectively (Fig. 2A). Similar to cultivar MH63, Se(VI) addition had much better inhibiting effect on the uptake of As(III) and As(V) by cultivar LYMZ than Se(IV) addition (Fig. 2A). In As(III)-spiked paddy soil, the addition of Se(IV) decreased the As(III) concentration in the roots and leaves of cultivar LYMZ by (12.26 ± 0.81)% and (46.17 ± 1.53)% respectively, and also decreased the As(V) concentration in the roots, stems, sheaths, leaves and bran of cultivar LYMZ by (16.78 ± 0.89)%, (47.07 ± 1.78)%, (42.88 ± 1.59)%, (21.25 ± 0.95)% and (2.43 ± 0.23)% respectively relative to the standalone As(III)-spiked treatment, (Fig. 2B). The addition of Se(VI) decreased the As(III) concentration in the sheaths and leaves of cultivar LYMZ by (10.11 ± 0.68)% and (47.92 ± 2.27)% respectively, and also decreased the As(V) concentration in the stems, sheaths, leaves and bran of cultivar LYMZ by (36.09 ± 1.43)%, (33.79 ± 1.62)%, (33.19 ± 1.69)% and (11.18 ± 0.59)% respectively relative to the standalone As(III)-spiked treatment (Fig. 2B). Different from low arsenic paddy soil and cultivar MH63, the inhibiting effect between the addition of Se(IV)/Se(VI) and the As(III)/As(V) uptake by cultivar LYMZ was significantly weakened relative to the standalone As(III)-spiked treatment (Fig. 2B), indicating that the antagonistic effect between the addition of Se(IV)/ Se(VI) and the As(III)/As(V) uptake depended on rice cultivars and the As concentration in soil. To our knowledge, no report described

Fig. 1. Effect of selenium on the concentrations of each arsenic species in rhizosphere pore water. A: low arsenic-level paddy soil without the addition of As(III)/As(V); B: As(III)/ As(V)-spiked paddy soil. Results are presented as mean ± standard deviation (n ¼ 4); NP-27, NP-51, NP-70 and NP-100 was regulated with selenium for 27, 51, 70 and 100 d respectively, and no rice was planted; MH63e27, MH63e51, MH63e70 and MH63-93 were regulated with selenium for 27, 51, 70 and 93 d, respectively; LYMZ-27, LYMZ-51, LYMZ70 and LYMZ-104 were regulated for 27, 51, 70 and 104 d, respectively; the detailed treatments of CT00, CT04, CT06, AT30, AT34, AT36, AT50, AT54 and AT56 were descripted in Materials and methods 2.2.

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Fig. 2. Effect of selenium on the concentrations of each arsenic species in different organs of rice plants at maturing stage. A: low arsenic-level paddy soil without the addition of As(III)/As(V); B: As(III)/As(V)-spiked paddy soil. Results are presented as mean ± standard deviation (n ¼ 4). The detailed treatments of CT00, CT04, CT06, AT30, AT34, AT36, AT50, AT54 and AT56 were descripted in Materials and methods 2.2.

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this kind of correlation within the whole growing stage of rice plants. In As(V)-spiked paddy soil, the addition of Se(IV) decreased the As(III) concentration in the roots, stems, sheaths, leaves, bran and kernel of cultivar LYMZ by (14.88 ± 0.72)%, (14.01 ± 0.63)%, (9.62 ± 0.61)%, (26.09 ± 1.06)%, (30.08 ± 1.79)% and (25.18 ± 1.46)% respectively, and also decreased the As(V) concentration in the roots, stems, sheaths, leaves and bran of cultivar LYMZ by (13.23 ± 0.76)%, (31.10 ± 1.33)%, (18.23 ± 0.64)%, (58.77 ± 2.84)% and (14.25 ± 0.65)% respectively relative to the standalone As(V)-spiked treatment (Fig. 2B). The addition of Se(VI) decreased the concentration of As(III) in the stems, sheaths, leaves, bran and kernel of cultivar LYMZ by (25.38 ± 0.87)%, (20.97 ± 0.72)%, (36.59 ± 1.03)%, (47.77 ± 1.56)% and (15.51 ± 0.53)% respectively, and also decreased the concentration of As(V) in the stems, sheaths, leaves and bran of cultivar LYMZ by (32.23 ± 0.69)%, (14.93 ± 0.58)%, (33.92 ± 0.97)% and (29.08 ± 0.94)% respectively relative to the standalone As(V)spiked treatment (Fig. 2B). Different from As(III)-spiked paddy soil, Se(VI) addition had better inhibiting effect on As(III) uptake, while Se(IV) addition had better inhibiting effect on As(V) uptake by cultivar LYMZ relative to the standalone As(V)-spiked treatment (Fig. 2B), indicating that their antagonistic effect between the addition of Se(IV)/Se(VI) and the As(III)/As(V) uptake also depended on As species in soil.

antagonism between the addition of Se(IV)/Se(VI) and the total concentration of As(III) and As(V) by rice plants also depended on rice cultivars, As species and concentration level in paddy soil. Although the uptake rate of methylated As species was much slower than that of As(III) or As(V), their mobility within the plant was substantially higher than that of As(III) or As(V) (Raab et al., 2007). It was reported that methylated As species was also transported into rice roots by the aquaporin Lsi1 (Li et al., 2009). As for cultivar LYMZ, that was true, the addition of Se(IV) decreased the total concentration of TMAO(V), DMA(V) and As(III) in As(III)spiked paddy soil, whereas the addition of Se(VI) increased the total concentration of TMAO(V), DMA(V) and As(III) in As(V)-spiked paddy soil (Table 1). However, the antagonism between the addition of Se(IV)/Se(VI) and the total concentration of TMAO(V) and DMA(V) by cultivar MH63 was different from that by cultivar LYMZ. The addition of Se(IV) decreased the total concentration of As(III) in cultivar MH63, but increased the total concentration of DMA(V) in cultivar MH63 in As(III)/As(V)-spiked paddy soil (Table 1). Therefore, there existed both synergistic and inhibiting effect between the addition of Se(IV)/Se(VI) and the total concentration of TMAO(V) and DMA(V), but the mechanism was unclear.

3.4. Effect of selenium regulation on the total concentration of each arsenic species in rice plants

In low arsenic paddy soil, the addition of Se(VI) significantly (p < 0.01) decreased the iAs transfer factor of stem-to-root, sheathto-root, leaf-to-root, bran-to-root and kernel-to-root in cultivars MH63 and LYMZ except that of kernel-to-root in cultivar LYMZ, while the addition of Se(IV) increased the iAs transfer factor of roots to the above-ground organs in both cultivar MH63 and cultivar LYMZ (Table 2). In As(III)-spiked paddy soil, the addition of Se(VI) also significantly (p < 0.01) decreased the iAs transfer factor of stem-to-root, sheath-to-root, leaf-to-root, bran-to-root and kernelto-root in cultivar MH63 and LYMZ except that of stem-to-root in cultivar MH63 and that of bran-to-root in cultivar LYMZ (Table 2). In As(V)-spiked paddy soil, the addition of Se(VI) only significantly (p < 0.01) decreased the iAs transfer factor of sheath-to-root and leaf-to-root in cultivar MH63, and the iAs transfer factor of stem-toroot in cultivar LYMZ (Table 2). Although the addition of Se(IV) significantly (p < 0.01) decreased the iAs transfer factor of leaf-toroot in cultivar MH63 in As(III)-spiked paddy soil, decreased the iAs transfer factor of roots to the above-ground organ in cultivar LYMZ except that of bran-to-root in As(III)-spiked paddy soil, and decreased the iAs transfer factor of stem-to-root, sheath-to-root and leaf-to-root in cultivar MH63 in As(V)-spiked paddy soil, its inhibiting effect on the iAs transfer factor of roots to the aboveground rice organs was lower than Se(VI) (Table 2). Our results were opposite to the short-term hydroponic experiments of Hu et al. (2014) and Camara et al. (2018), which reported that Se(IV) was more effective to mitigate As translocation from rice roots to the above-ground rice organs than Se(VI).

Our results showed that there existed good antagonistic effect between the addition of Se(IV)/Se(VI) and the uptake of As(III)/ As(V) by rice organs, but this antagonism depended on rice cultivars, As concentration and As species in paddy soil (Fig. 2). After As(III) was ingested into rice roots by silicon transporters Lsi1 (Ma et al., 2008), it might be accumulated in rice roots, excreted out of rice roots or further transported into the aboveground rice organs by silicon transporters Lsi2 (Zhao et al., 2009). After As(V) was transported into rice roots by the phosphate transporters (Zheng et al., 2013), it might be accumulated in rice roots, reduced into As(III) by As(V) reductase and excreted out of rice roots (Xu et al., 2007), or further transported up into the aboveground rice organs by the phosphate transporters (Zhao et al., 2009). Therefore, the total concentration of each arsenic species, accumulated in rice plants, was the results of the dynamic equilibrium from their uptake, transformation, excretion and translocation within different rice organs, controlled by its species and the competitive/synergistic uptake with other mineral elements (Wang et al., 2002). In low arsenic paddy soil, the addition of Se(IV) or Se(VI) significantly (p < 0.01) decreased the total concentration of As(III) and As(V) in cultivar MH63, moreover, Se(VI) addition had better inhibiting effect on As(III) concentration than Se(IV) addition, whereas Se(IV) addition had better inhibiting effect on As(V) concentration than Se(VI) addition. But the addition of Se(IV) or Se(VI) increased the total concentration of As(III) and As(V) in cultivar LYMZ (Table 1). In As(III)-spiked paddy soil, the antagonism between the addition of Se(IV)/Se(VI) and the uptake of As(III)/As(V) by cultivar MH63 was similar to that in low arsenic paddy soil. However, the addition of Se(IV) significantly (p < 0.01) decreased the total concentration of As(III) and As(V) in cultivar LYMZ (Table 1). In As(V)-spiked paddy soil, the antagonism between the addition of Se(IV)/Se(VI) and the As(III) uptake by cultivar MH63 was also similar to that in low arsenic paddy soil, but only Se(VI) addition decreased the As(V) uptake by cultivar MH63. As for cultivar LYMZ, only Se(IV) addition decreased the total concentration of As(III) and As(V) in cultivar LYMZ (Table 1). Therefore, the

3.5. Effect of selenium regulation on inorganic arsenic translocation from roots to above-ground organs

3.6. Effect of selenium regulation on arsenic toxicity to rice plants Selenium had different effects on chlorophyll SPAD value of rice plants, plants height, roots length, dried weight of different rice organs, average number of rice panicles and grain yield (Figs. S4eS8 in SI). At tillering and booting stages, whether As(III)/As(V) was spiked into paddy soil or not, Se(VI) had better renovation effect on chlorophyll SPAD value of rice cultivars MH63 and LYMZ (Fig. S4 in SI), while Se(IV) had the opposite results on the plants height of both rice cultivars (Fig. S5 in SI). At maturing stage, Se(VI) had the best renovation effect on roots length of rice cultivar LYMZ in As(III)-spiked paddy soil (Fig. S6 and Fig. S8B in SI), had the best

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Table 1 Effect of selenium on arsenic species uptake in rice plant at maturing stage. Different letters within the same column indicated significant differences among Se(IV) or Se(VI) treatments under As(III)/As(V)-spiked soil or not (p < 0.01). Data are mean ± SD (n ¼ 4). Treatments As added (mg/kg) Se added (mg/kg) Total concentration of each arsenic species in rice plant (mg/kg root FW) Cultivar MH63

CT00 CT04 CT06 AT30 AT34 AT36 AT50 AT54 AT56 a

0 0 0 50 50 50 50 50 50

TMAO(V) DMA(V)

As(III)

As(V)

TMAO(V)

DMA(V)

As(III)

As(V)

a

0.43 ± 0.03 A 0.17 ± 0.01 B 0.13 ± 0.01C 10.35 ± 0.09 A 2.60 ± 0.22 B 1.98 ± 0.16C 9.91 ± 0.78 A 2.95 ± 0.08 B 2.60 ± 0.07C

1.18 ± 0.07 A 0.65 ± 0.04C 1.06 ± 0.04 B 98.29 ± 7.33 A 52.69 ± 4.22C 74.84 ± 5.39 B 34.95 ± 1.64 B 47.34 ± 2.78 A 30.82 ± 1.17C

0.01 ± 0.00 A 0.01 ± 0.00 A 0.01 ± 0.00 A 0.32 ± 0.04 A 0.18 ± 0.01 B 0.04 ± 0.01C 0.07 ± 0.01C 0.17 ± 0.01 A 0.12 ± 0.01 B

0.01 ± 0.00 A n.d. B n.d. B 0.54 ± 0.05 A 0.17 ± 0.01 B 0.15 ± 0.01C 0.22 ± 0.01 B 0.22 ± 0.01 B 0.29 ± 0.01 A

0.78 ± 0.08 B 1.13 ± 0.10 A 0.91 ± 0.06 B 28.38 ± 2.43 A 21.28 ± 2.07 B 27.48 ± 2.46 A 23.69 ± 1.06 B 22.94 ± 1.89 B 30.12 ± 2.65 A

2.12 ± 0.20C 2.71 ± 0.13 B 3.45 ± 0.12 A 118.31 ± 7.97 B 95.91 ± 6.01C 160.10 ± 6.73 A 161.15 ± 7.18 A 141.01 ± 6.82 B 168.48 ± 7.89 A

n.d. A n.d. A n.d. A n.d. A n.d. A n.d. A n.d. A n.d. A n.d. A

0 4 4 0 4 4 0 4 4

Cultivar LYMZ

n.d. A n.d. A n.d. A 0.07 ± 0.01 B 0.11 ± 0.01 A 0.03 ± 0.00C n.d. B 0.07 ± 0.01 A n.d. B

Not detected.

Table 2 Effect of selenium on the transfer factor of inorganic arsenic in rice plants at maturing stage. Different letters within the same column indicated significant differences among Se(IV) or Se(VI) treatments under As(III)/As(V)-spiked soil or not (p < 0.01). Data are mean ± SD (n ¼ 4). Treatments

Transfer factor of inorganic arsenic Cultivar MH63

CT00 CT04 CT06 AT30 AT34 AT36 AT50 AT54 AT56

Cultivar LYMZ

Stem to root

Sheath to root

Leaf to root

Bran to root

Kernel to root

Stem to root

Sheath to root

Leaf to root

Bran to root

Kernel to root

0.28 ± 0.01 B 0.41 ± 0.01 A 0.16 ± 0.01C 0.02 ± 0.00C 0.03 ± 0.00 B 0.04 ± 0.00 A 0.07 ± 0.01 A 0.05 ± 0.00 B 0.07 ± 0.00 A

0.14 ± 0.01 B 0.52 ± 0.02 A 0.10 ± 0.01C 0.02 ± 0.00 B 0.03 ± 0.00 A 0.01 ± 0.00C 0.12 ± 0.01 A 0.04 ± 0.00C 0.05 ± 0.00 B

0.06 ± 0.01 B 0.13 ± 0.01 A 0.03 ± 0.00C 0.02 ± 0.00 A 0.02 ± 0.00 A 0.01 ± 0.00 B 0.08 ± 0.00 A 0.03 ± 0.00C 0.07 ± 0.00 B

0.02 ± 0.00 A 0.02 ± 0.00 A 0.01 ± 0.00 B 0.00 ± 0.00 A 0.00 ± 0.00 A 0.00 ± 0.00 A 0.00 ± 0.00 A 0.00 ± 0.00 A 0.00 ± 0.00 A

0.01 ± 0.00 B 0.04 ± 0.00 A 0.00 ± 0.00C 0.00 ± 0.00 A 0.00 ± 0.00 A 0.00 ± 0.00 A 0.00 ± 0.00 A 0.00 ± 0.00 A 0.00 ± 0.00 A

0.66 ± 0.02 B 0.82 ± 0.03 A 0.23 ± 0.01C 0.03 ± 0.00 A 0.01 ± 0.00 B 0.01 ± 0.00 B 0.01 ± 0.00 B 0.02 ± 0.00 A 0.01 ± 0.00 B

0.13 ± 0.01 B 0.22 ± 0.01 A 0.07 ± 0.01C 0.02 ± 0.00 A 0.01 ± 0.00 B 0.01 ± 0.00 B 0.01 ± 0.00 B 0.02 ± 0.00 A 0.01 ± 0.00 B

0.27 ± 0.01 B 0.46 ± 0.01 A 0.13 ± 0.01C 0.05 ± 0.00 A 0.02 ± 0.00 B 0.01 ± 0.00C 0.03 ± 0.00 A 0.03 ± 0.00 A 0.03 ± 0.00 A

0.02 ± 0.00 B 0.05 ± 0.00 A 0.01 ± 0.00C 0.00 ± 0.00 A 0.00 ± 0.00 A 0.00 ± 0.00 A 0.00 ± 0.00 A 0.00 ± 0.00 A 0.00 ± 0.00 A

0.02 ± 0.00 B 0.04 ± 0.00 A 0.02 ± 0.00 B 0.00 ± 0.00 A 0.00 ± 0.00 A 0.00 ± 0.00 A 0.00 ± 0.00 A 0.00 ± 0.00 A 0.00 ± 0.00 A

renovation effect on average number of rice panicles of cultivar LYMZ in low arsenic paddy soil (Fig. S8A in SI), also had better renovation effect on grain yield of rice cultivar LYMZ in As(III)/ As(V)-spiked paddy soil than Se(IV) (Fig. S8B in SI), but Se(IV) had the opposite results on dried weight of roots and sheaths of both indica cultivars in As(III)/As(V)-spiked paddy soil (Fig. S7 in SI), also had the opposite results on average number of rice panicles of cultivar LYMZ in As(III)/As(V)-spiked paddy soil (Fig. S8A in SI). Therefore, the effect of Se on As toxicity to rice plants was also dependent on rice cultivars, As species and concentration level in paddy soil. 4. Conclusions A pot experiment was designed to investigate the effect of Se(IV) or Se(VI) addition on As(III) or As(V) toxicity to different rice cultivars, and the uptake and transportation of As species from paddy soil to different rice organs. The results showed that the existence of Se(IV) or Se(VI) could significantly decrease the As(V) concentrations in pore water of soils, and thus inhibited the As(V) uptake by rice roots. However, the existence of Se(IV) or Se(VI) didn't decrease the As(V) concentration in rhizosphere pore water of cultivar MH63 or LYMZ. The experimental results also indicated that there are good antagonistic effect existing between the addition of Se(IV)/Se(VI) and the uptake of As(III)/As(V) by rice plants in low As paddy soil, but the antagonism between Se(IV) or Se(VI) nutrient and the uptake of As(III) and As(V) depended on rice cultivars, As species and As concentration level in soil. Moreover, there existed both synergistic and inhibiting effects between the addition of Se(IV) or Se(VI) nutrient and the uptake of TMAO(V) and DMA(V), but the mechanism was unclear. Therefore, there is a need

for further study about the effects of Se nutrition in soil on As species accumulation in more rice cultivars and As species transportation from different As contamination level soil to rice grains before practical applications in field soil. Conflict of interest The authors have declared no conflict of interest. Acknowledgements The research was supported by Natural Science Foundation of China (grant numbers 21677033 and 21677034); Fujian Provincial Project of Science and Technology (grant numbers 2017Y0002); Project of China Tobacco Yunnan Industrial Co. Ltd. (grant number 2016YL03); Project of Yunnan Company of China Tobacco Corporation (grant number 2017YN06 and 2016YN28). Appendix A. wSupplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.chemosphere.2019.124712. References Abedin, M.J., Feldmann, J., Meharg, A.A., 2002. Uptake kinetics of arsenic species in rice plants. Plant Physiol. 128, 1120e1128. Abdein, M.J., Meharg, A.A., 2002. Relative toxicity of arsenite and arsenate on germination and early seedling growth of rice (Oryza sativa L.). Plant Soil 243, 57e66. Camara, A.Y., Wan, Y., Yu, Y., Wang, Q., Li, H., 2018. Effect of selenium on uptake and translocation of arsenic in rice seedlings (Oryza sativa L.). Ecotoxicol. Environ. Saf. 148, 869e875.

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