Sulfate application decreases translocation of arsenic and cadmium within wheat (Triticum aestivum L.) plant

Journal Pre-proof Sulfate application decreases translocation of arsenic and cadmium within wheat (Triticum aestivum L.) plant

Gaoling Shi, Haiying Lu, Huan Liu, Laiqing Lou, Pingping Zhang, Guicheng Song, Huimin Zhou, Hongxiang Ma PII:

S0048-9697(20)30175-3

DOI:

https://doi.org/10.1016/j.scitotenv.2020.136665

Reference:

STOTEN 136665

To appear in:

Science of the Total Environment

Received date:

25 November 2019

Revised date:

31 December 2019

Accepted date:

11 January 2020

Please cite this article as: G. Shi, H. Lu, H. Liu, et al., Sulfate application decreases translocation of arsenic and cadmium within wheat (Triticum aestivum L.) plant, Science of the Total Environment (2018), https://doi.org/10.1016/j.scitotenv.2020.136665

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© 2018 Published by Elsevier.

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Sulfate application decreases translocation of arsenic and cadmium within wheat (Triticum aestivum L.) plant Gaoling Shia,c,d, Haiying Lub, , Huan Liuc, Laiqing Louc, Pingping Zhanga, Guicheng Songa, Huimin Zhoua, Hongxiang Maa, 

a

Provincial Key Laboratory of Agrobiology, and Institute of Food Crops, Jiangsu Academy of

Institute of Agricultural Resources and Environment, Jiangsu Academy of Agricultural Sciences,

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b

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Agricultural Sciences, Nanjing, 210014, P.R. China.

Nanjing, 210014, P.R. China.

College of Life Sciences, Nanjing Agricultural University, Nanjing, 210095, P.R. China.

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School of the Environment and Safety Engineering, Jiangsu University, Zhenjiang, 212013, P.R.

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c

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China.



Corresponding author. Corresponding author. E-mail addresses: [email protected] (H. Lu), [email protected] (H. Ma), [email protected] (G. Shi). 

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Abstract Arsenic (As) and cadmium (Cd) typically exhibit divergent fates in soil, which complicates efforts to decrease As and Cd accumulation in the edible parts of crops. Here, we performed pot experiments to examine the effect of sulfate application on As and Cd accumulation in the grain of wheat grown in contaminated soil. Compared to the control (no sodium sulfate addition), application of 120 mg kg−1 sodium sulfate decreased the rhizosphere soil pH from 7.27 to 7.10 and increased the soil extractable Cd concentration; however, it did not significantly influence the soil extractable As concentration.

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However, sodium sulfate addition decreased As and Cd concentrations in wheat grain, in association

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with decreased As and Cd translocation from root and straw to grain, rather than from soil to root. Furthermore, sodium sulfate addition significantly decreased membrane lipid peroxidation and

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enhanced photosynthesis, while increasing the uptake of nitrogen, phosphorus, and sulfur. These

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effects increased the growth and grain weight of plants grown in As and Cd co-contaminated soil. Our findings provide insight into the mechanisms by which sulfate modulates As and Cd uptake and

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translocation in wheat; moreover, our findings will enable formulation of strategies to decrease As

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and Cd concentrations in the grain of wheat grown in As and Cd co-contaminated soil.

1. Introduction

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Keywords: Arsenic; Cadmium; Sulfate; Wheat; Phosphorus

Arsenic (As) and cadmium (Cd) have a negative impact on human health and are ranked first and seventh, respectively, on the priority list of hazardous substances compiled by the Agency for Toxic Substances and Disease Registry (ATSDR, 2017). Arsenic and Cd have also been designated as group 1 human carcinogens (IARC, 2019). Chronic exposure to As can lead to a variety of diseases, such as lung, skin, and bladder cancers, as well as cardiovascular disease, diabetes, neurological disorders, and dermal conditions (Smith and Steinmaus, 2009; Ye et al., 2012). Moreover, long-term exposure to Cd can lead to serious health problems, including kidney disease, lung disease, and Itai-Itai disease (Inaba et al., 2005; Satarug et al., 2010; Liu et al., 2015). In general, most As and Cd consumed by humans originates directly or indirectly from contaminated food crops. Arsenic and Cd concentrations in agricultural soils have increased in recent decades due to mining, industrial processing, irrigation with contaminated groundwater, and the use of pesticides and 2

Journal Pre-proof chemical fertilizers (Liu et al., 2010a; Rizwan et al., 2016; Yu et al., 2016). The concentrations of As and Cd are elevated in the edible parts of crops grown in contaminated soil (Liu et al., 2010a; Chi et al., 2018; Rezapour et al., 2019). Therefore, lowering As and Cd concentrations in the edible parts of food crops would decrease As and Cd intake by humans. Wheat (Triticum aestivum) is an important staple food and ranks first in terms of global consumption; 748 million tonnes are consumed annually, compared to 510 million tonnes of rice (FAO, 2019). Compared with other cereals such as maize and barley, wheat accumulates more Cd in the edible parts of the plant (Yang et al., 2014; Adams et al., 2004; Rizwan et al., 2016). Therefore,

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based on the amount of wheat consumed and the concentration of Cd in wheat grain, it has been estimated that wheat is a major source of Cd intake by humans (Greger and Löfstedt, 2004).

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Although the As level is lower in wheat than in rice (Williams et al., 2007; Su et al., 2010; Bhattacharya et al., 2010), high concentrations of As have also been detected in the grain of wheat

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plants grown in soils with an elevated level of As (Zhao et al., 2010; Duncan et al., 2017). Moreover,

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As in wheat grain mainly exists in its inorganic form (Zhao et al., 2010; Shi et al., 2013; Rasheed et al., 2018), which is more toxic to humans than organic forms such as dimethylarsinate and

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monomethilarsonate (Styblo et al., 2000; Sun et al., 2008). The chronic health risks associated with dietary intake of inorganic As are reportedly higher for intake from wheat than for intake from rice in

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some areas, such as the Santa Fe Province of Argentina (Sigrist et al., 2016) and some districts of Pakistan (Rasheed et al., 2018). Thus, there is a critical need to decrease As and Cd accumulation in

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the grain of wheat plants grown in As and Cd co-contaminated soils. Several mitigation strategies have been employed to decrease As and Cd accumulation in the edible parts of crops (Hu et al., 2013; Shan et al., 2016; Duan et al., 2017). However, because of the divergent geochemical behavior of As and Cd in soil, the decrease of As and Cd accumulation in crops in co-contaminated fields is challenging (Duan et al., 2017; Qiao et al., 2018). For example, liming decreases Cd, but not As, accumulation in crops (Bolan et al., 2003; Zhu et al. 2016). In addition, the application of biochar and phosphorous (P) fertilizer, as well as water management, exerts contrasting effects on As and Cd accumulation in plants (Arao et al. 2009; Beesley et al., 2010; Hu et al. 2013; Duan et al., 2017). Sulfur (S) is an essential nutrient for plant growth and is considered the fourth major nutrient element after nitrogen (N), P, and potassium (K) (Tao et al., 2018). Sulfur application affects As and Cd uptake, translocation, and accumulation in plants (Zhang et al., 2011; Dixit et al., 2015; Liang et al., 2016; Cao et al., 2018). Sulfur application decreases the bioavailability of As and Cd to rice by

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Journal Pre-proof enhancing iron plaque formation on the root surface (Hu et al., 2007; Lee et al., 2013; Cao et al., 2018). In addition, S application promotes the precipitation of Cd as CdS in waterlogged paddy soils, decreasing soil Cd availability (Arao et al. 2009; de Livera et al., 2011; Fulda et al., 2013). Furthermore, S has a robust effect on As and Cd translocation in plants. Sulfur application suppresses As and Cd translocation to rice shoot and grain by increasing the biosynthesis of S-containing compounds, including glutathione and phytochelatins (Fan et al., 2010; Duan et al., 2011; Cao et al., 2018). Liang et al. (2016) reported that S application decreased Cd translocation from root to shoot in Brassica chinensis and attributed this effect to increased S assimilation and glutathione

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metabolism. Therefore, S application is an effective and safe means of decreasing the As and Cd

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concentrations in rice grain.

Wheat and rice roots differ markedly in the genesis and appearance of aerenchyma (Prade and

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Trolldenier, 1990). Although iron plaques form on the surface of rice roots, this does not occur on the surface of wheat roots (Tripathi et al., 2014). In addition, sulfate can be transformed into sulfion (S2-)

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under anaerobic soil conditions (Murase and Kimura, 1997; de Livera et al., 2011). Thus, when a

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paddy field is flooded, increased sulfate supply could increase Cd precipitation as CdS, resulting in a decrease in rice Cd uptake (Fan et al., 2010; Zhang et al., 2019). In contrast, wheat is typically grown

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in aerobic soil, increasing sulfate concentration in aerobic soil would promote Cd formation as CdSO4, which is soluble in soil solution (McLaughlin et al., 1998; Arao et al. 2009). Thus, there is a need to investigate the effect of sulfate on the bioavailability of As and Cd to wheat plants. Previous

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studies of the effect of S application on As and Cd accumulation in plants investigated a single element, such as As or Cd. However, As and Cd coexist in most contaminated soils (Wang et al., 2016; Duan et al., 2017; Qiao et al., 2018); therefore, the interactions among As, Cd, and S in soil–plant systems are more complex than the simple interactions of As/Cd with S. The effects of sulfate application on As and Cd accumulation in wheat grain, as well as the underlying mechanisms of these effects, remain unclear. Here, we determined the effect of sulfate application on the accumulation of As and Cd in wheat grain, then assessed the mechanisms of sulfate-mediated As and Cd accumulation in wheat grown in As and Cd co-contaminated soil. We also evaluated the effect of sulfate on As and Cd-induced changes in plant growth, photosynthesis, soil As and Cd mobilization, As and Cd uptake and translocation, and N, P, and S uptake in wheat.

2. Materials and Methods 4

Journal Pre-proof 2.1. Soil and plant materials Two commercial winter wheat (Triticum aestivum L.) cultivars, Jinmai 85 (JM85) and Mianmai 45 (MM45), which differ in grain Cd accumulation (Shi et al., 2015), were used in this study. Soil for the pot experiment was collected from the surface layer (0–20 cm) of farmland in Shantou, Guangdong Province; this soil was contaminated with both As and Cd due to past mining activities (Liu et al., 2010a; Yu et al., 2016). Soil was air-dried, mixed thoroughly, and passed through a 4.0-mm mesh before use. The basic physical and chemical properties of the soil were analyzed in accordance with the routine analytical methods described in Soil and Agricultural Chemistry

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Analysis (Bao, 2000). In short, the soil pH was measured at a soil-to-water ratio of 1:2.5 (w/v) using

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a pH meter. Soil organic carbon and total N were determined by potassium dichromate and Kjeldahl method, respectively. Total S was digested by Mg(NO3)2 and available S was extracted by CaCl2, and

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then determined by turbidimetric method. The soil texture was determined using the procedure

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described by Avery and Bascomb (1982). Total P, K, As, Cd, Cu, Pb, and Zn were measured by inductively coupled plasma-optical emission spectroscopy after aqua regia digestion (Zhao et al.,

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2010). The soil was clay loam, lightly alkaline (pH 7.4), and contained 17.8 g kg−1 organic matter. The total As, Cd, Cu, Pb, and Zn concentrations were 146, 3.0, 53, 68, and 46 mg kg−1, respectively.

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The total N, P, K, and S concentrations were 1.52, 1.13, 12.5, and 0.332 g kg−1, respectively. The

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concentration of CaCl2-extractable S was 13.1 mg kg−1. 2.2 Experimental design

Pot experiments were carried out during the wheat-growing season (from the end of October 2016 to the end of May 2017) under open-air conditions at Pailou Experimental Station of Nanjing Agricultural University, Nanjing, China. Each pot was filled with 6 kg of air-dried soil. There were six treatments comprising two wheat cultivars and three S levels. Sulfate was applied as Na2SO4 solution at 0 (control), 60 (S60), and 120 (S120) mg kg−1. One half of S was added to the soil as a basal dose and equilibrated for 7 days prior to planting, one quarter was applied at the wheat-jointing stage (the first node of the stem becomes visible), and the rest was applied at the booting stage (the head begins to form inside the flag leaf). The moisture content of the soil was maintained at 65–70% of the field water-holding capacity. Wheat seeds were surfaced-sterilized with 3% H2O2 (v/v) solution for 10 min and rinsed in

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Journal Pre-proof deionized water. Initially, eight seeds were sown in each pot and three uniform seedlings were retained in each pot at 21 days after germination. Basal fertilizer was applied at 160 mg N (as urea), 40 mg P (as KH2PO4), and 120 mg K (as KCl and KH2PO4) kg−1 soil in each pot, 5 days prior to sowing. N, P, and K fertilizers were applied at 80, 20, and 60 mg kg−1, respectively, at the jointing stage. The pots were arranged in a completely randomized design in two groups of 18 pots (six treatments each of three replicates), for a total of 36 pots. One group was sampled destructively at the flowering stage and the other at maturity. Pots were placed on the field and rearranged

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periodically to minimize the influence of environmental gradients.

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2.3. Sampling and measurements

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At the flowering stage, wheat flag leaves from three randomly selected pots per treatment were subjected to measurement of the net photosynthetic rate, stomatal conductance, intercellular CO2

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concentration, and transpiration rate, from 9:00 to 11:30 am on a sunny day, using a LiCor-6400

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photosynthesis system (Li-Cor Biosciences, Lincoln, NE, USA). All measurements were conducted under photosynthetically active radiation of 1,200 μmol (photon) m−2 s−1 and 380 μmol mol−1 CO2.

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Plants were harvested after measurement of leaf gas-exchange parameters; the flag leaves were detached, rinsed in deionized water, blotted dry, weighed, frozen in liquid nitrogen, and prepared for

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lipid peroxidation analysis.

The level of lipid peroxidation was estimated by measuring the malondialdehyde (MDA) concentration as described by Hodges et al. (1999), with minor modifications. Briefly, 0.50 g of fresh sample was ground in 5 mL of 5% trichloroacetic acid. The homogenate was centrifuged at 5000 × g for 10 min; 2 mL of the supernatant were mixed with 4 mL of 0.67% (w/v) thiobarbituric acid in 10% trichloroacetic acid, incubated for 30 min in a boiling-water bath, and rapidly cooled in an ice bath. The supernatant was centrifuged at 12,000 × g for 10 min; then, the absorbances at 400, 532, and 600 nm were measured. The concentration of MDA was calculated as follows: C (μmol L−1) = [6.45 × (A532 − A600)] − [0.56 × A450], where C is the MDA concentration in supernatant (Zhao et al., 2017). The MDA concentration in plant samples was expressed as nmol g−1 fresh weight. At maturity, the second group of plants was harvested and three plants per replicate were sampled; the root, straw, and grain were separated. The harvested plants were washed thoroughly

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Journal Pre-proof with tap water followed by deionized water; the roots were soaked in 5 mM CaCl2 solution for 15 min to remove adherent metal ions (Shan et al. 2016). All plant parts were washed in deionized water; then, they were dried in an oven at 65°C to constant weight. The dried samples were weighed and ground to pass through a 100-mesh sieve for elemental analysis. Samples of rhizosphere soil were collected at that time. The rhizosphere soils were collected following the method of Szmigielska et al. (1996). Briefly, wheat plants were removed from the pots and the soil loosely adhering to the roots was gently shaken off back into each pot. Soil adhering to the roots was washed off with deionized water and this soil represented the rhizosphere soil. The soil samples were air-dried, gently

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disaggregated, and passed through a 10-mesh nylon sieve for pH determination. Portions of each soil

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sample were gently crushed, passed through a 100-mesh nylon sieve, and prepared for elemental analysis.

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Soil available As and Cd were extracted with 0.01 M CaCl2 using a soil-to-solution ratio of 1:10

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(w/v), as described by Luo et al. (2012). To assay the concentrations of As, Cd, and P, 0.25-g

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powdered samples were digested with HNO3:H2O2 (1:1, v/v) at 125°C, as described by Tao et al. (2006). As and Cd concentrations were determined by inductively coupled plasma mass spectroscopy

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(iCAP QC, Thermo Fisher Scientific, Waltham, MA, USA), and the total P concentration was determined by inductively coupled plasma-optical emission spectroscopy (Optima 2100DV,

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PerkinElmer, Waltham, MA, USA). The total S and N concentrations in plant samples were determined using an elemental analyzer (Vario Macro Cube, Elementar, Langenselbold, Germany). To verify the accuracy of the digestion and analysis procedure, standard reference materials of rice flour (NIST-SRM 1568b) and orange leaves (GBW 10020, from the National Research Center for Standards, China) were used in the analysis. The recoveries of As, Cd, N, P, and S were 90–96%, 102–107%, 103–110%, 98–101%, and 99–105%, respectively. 2.4. Data analysis Data shown are the means ± standard deviations of three independent biological replicates. Data were analyzed using Excel 2010 (Microsoft, Redmond, WA, USA) and SPSS 16.0 for Windows (Chicago, IL, USA). Differences among treatments were evaluated by one-way analysis of variance, followed by Duncan’s multiple comparison test (p ≤ 0.05). The As, Cd, N, P, and S contents (mg) of plant parts were calculated by multiplying their concentrations by the corresponding biomass.

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3. Results 3.1. Soil pH and heavy metal/metalloid bioavailability As shown in Table 1, sodium sulfate application had a significant (p ≤ 0.05) effect on the pH of rhizosphere soil. Compared to the control (S0), application of 120 mg kg−1 sodium sulfate (S120) decreased the rhizosphere soil pH from 7.26 to 7.09 and 7.28 to 7.11 for JM85 and MM45, respectively, while 60 mg kg−1 sodium sulfate (S60) did not significantly influence soil pH. Moreover, the CaCl2-extractable Cd concentration in rhizosphere soil was increased by 32% with

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application of S120, but unchanged with application of S60, compared to the control. The CaCl2-extractable As concentration in rhizosphere soil was not significantly affected by sodium

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sulfate treatments.

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3.2. Plant biomass

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The effects of sodium sulfate application on the dry biomass of wheat grown in As and Cd co-contaminated soil are shown in Fig. 1. The plant root, straw, and grain weights of both cultivars

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increased with increasing sodium sulfate concentration. On average (based on assessment of two wheat cultivars, JM85 and MM45), application of S120 increased the dry weights of grain, straw,

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and root by 25%, 25%, and 19%, respectively, compared to the control.

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3.3. Photosynthetic gas-exchange parameters The net photosynthetic rate, stomatal conductance, intercellular CO2 concentration, and Tr values are shown in Fig. 2. Compared to the control, application of S60 significantly (p ≤ 0.05) increased the net photosynthetic rate, stomatal conductance, and Tr values of both cultivars, with the exception of the net photosynthetic rate of cultivar JM85, which was significantly increased only with application of S120. The net photosynthetic rate, stomatal conductance, and Tr values were increased by 14%, 38%, and 29%, respectively, with application of S60, whereas they were increased by 23%, 59%, and 35% with application of S120. However, the intercellular CO2 concentration value did not differ significantly between sodium sulfate treatments. Therefore, the increased photosynthesis in sulfate-treated wheat plants grown in As and Cd co-contaminated soil might have been due to nonstomatal factors. 3.4. Lipid peroxidation

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Journal Pre-proof The concentration of MDA is an indicator of lipid peroxidation and is used to estimate the magnitude of oxidative stress. As shown in Fig. 3, the leaf MDA concentrations of both cultivars decreased with increasing sodium sulfate concentration. On average, the MDA concentrations were decreased by 19% and 27% following applications of S60 and S120, respectively, compared to the control. 3.5. As and Cd concentrations in wheat plants Fig. 4 shows the As and Cd concentrations in the root, straw, and grain of sulfate-treated wheat

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plants. Sodium sulfate application significantly (p ≤ 0.05) affected the root and grain As and Cd concentrations: the root As and Cd concentrations significantly increased, while those in grain

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significantly decreased, with increasing sodium sulfate application. Compared to the control, the

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average root As and Cd concentrations of the two cultivars increased by 58% and 39%, respectively, with application of S120. In contrast, the grain As and Cd concentrations decreased by 23% and 24%,

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respectively, with application of S120. The straw As and Cd concentrations were not significantly

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affected by sodium sulfate treatment, with the exception of the straw Cd concentration in MM45, which was significantly increased with application of S60, compared to the control.

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3.6. As and Cd translocation in wheat plants

The translocation of As and Cd in wheat plants was evaluated by measurement of the As and Cd

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concentration ratios in plant parts (Fig. 5a, b and Fig. 6a, b) and the percentage total As or Cd uptake distributed to straw and grain (Fig. 5c, d and Fig. 6c, d). Sodium sulfate application significantly (p ≤ 0.05) decreased As and Cd translocation from roots to above-ground parts, as well as from straw to grain (Figs. 5 and 6). The grain-to-straw and straw-to-root As concentration ratios decreased with increasing sodium sulfate application. The percentage of As in grain changed in a manner consistent with the grain-to-straw concentration ratio. In contrast, the percentage of As in root increased with increasing sodium sulfate application. Similar to As, the grain-to-straw Cd concentration ratio and percentage of Cd in grain were significantly (p ≤ 0.05) decreased by sodium sulfate application. The percentage of Cd in root was significantly increased with application of S120, compared to the control. However, the Cd straw-to-root concentration ratio did not differ significantly between sodium sulfate treatments and the control. 3.7. Uptake of N, P, and S 9

Journal Pre-proof As shown in Fig. 7, sodium sulfate application significantly (p ≤ 0.05) affected total N, P, and S uptake by wheat plants grown in As- and Cd-contaminated soil. Compared to the control, sodium sulfate addition significantly increased total N, P, and S uptake by both cultivars. On average, total N uptake was increased by 25% and 33%, total P uptake was increased by 30% and 37%, and total S uptake was increased by 57% and 68% with application of S60 and S120, respectively. Sodium sulfate application increased N, P, and S uptake explained by increase not only in biomass but also in the concentration of N, P, and S in wheat plants (Fig. 8). The concentrations of S and P in wheat root,

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with sulfate application, compared to the control (Fig. 8).

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straw, and grain, as well as the concentration of N in root and straw, were significantly increased

4. Discussion

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Sulfur is an essential element for plant growth and function. Moreover, S is critical for the

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structure and function of proteins and enzymes, as well as for plant defense against abiotic and biotic stresses (Zhao et al., 1999; Capaldi et al., 2015). Sulfur interacts strongly with As and Cd in

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soil–plant systems (Hu et al., 2007; Fan et al., 2010; Duan et al., 2011; Zhang et al., 2019). However, the behaviors of As and Cd in soils are typically divergent, and the influences of S on plant growth

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and As and Cd accumulation in wheat plants grown in As and Cd co-contaminated soil are unknown.

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In this study, sulfate application was found to increase wheat growth and decrease As and Cd accumulation in wheat grain. The role of sulfate in wheat growth and heavy metal/metalloid accumulation in wheat plants is discussed in detail below. Arsenic and Cd are non-essential and toxic to plants. Excess As and Cd inhibit plant growth by decreasing gas exchange, altering cellular ultrastructure, increasing oxidative stress, and decreasing mineral nutrient uptake (Farooq et al., 2013; Kollárová et al., 2019, Murtaza et al., 2019; Abbas et al., 2018; Huang et al., 2019). Our results showed that sodium sulfate addition significantly decreased lipid peroxidation of cellular membranes (Fig. 3), enhanced photosynthesis (Fig. 2), and increased N, P, and S uptake (Fig. 7) in wheat plants grown in As and Cd co-contaminated soil. These changes likely contributed to increased wheat growth and grain yield. Similarly, sulfate application has been found to increase plant growth through the decrease of oxidative stress caused by As (Dixit et al., 2015) and Cd (Liang et al., 2016). The increased wheat growth following application of sulfate may also be associated with the increased plant S uptake (Fig. 7), as well as increased glutathione and 10

Journal Pre-proof phytochelatin synthesis (Fan et al., 2010; Dixit et al., 2015; Cao et al., 2018). Phytochelatins is well known to detoxify As and Cd in plants by chelation and subsequent compartmentalization into vacuoles; these processes also decrease the translocation of As and Cd (Dixit et al., 2015; Cao et al., 2018; Liu et al., 2010b). Furthermore, sodium sulfate application increased the P concentrations in wheat root, straw, and grain (Fig. 8); these changes may be linked to the increased plant growth, because an increased intracellular P concentration is a mechanism by which plants establish tolerance to the toxicity of As (Lee et al., 2003; Shi et al., 2019). Therefore, when wheat plant grown in As and Cd contaminated soils, sulfate is much more than a simple nutrient, playing an important protective

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role against these two toxic elements.

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Consistent with the findings reported by McLaughlin et al. (1998) and Zhao et al. (2003), sulfate application increased soil Cd bioavailability in the rhizosphere. This is potentially because a

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considerable proportion of Cd in soil is in complex with sulfate ions under aerobic conditions, and

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the CdSO4 complex is soluble in water (McLaughlin et al., 1998; Zhao et al., 2003; Wang et al.,

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2019). Alternatively, Cd mobilization may have been increased by sulfate-induced pH changes in the rhizosphere. The rhizosphere soil pH was decreased from 7.27 to 7.10 with application of S120

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(Table 1), which altered the Cd distribution in soil fractions and increased soil Cd mobilization (Wang et al., 2016; Tahervand and Jalali, 2017; Zhang et al., 2019). Soil pH is also an important

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determinant of As bioavailability. Generally, soil As bioavailability increases with increasing soil pH within the normal range (Dixit and Hering, 2003; Yamaguchi et al. 2011). However, in the present study, rhizosphere As bioavailability was not decreased by sulfate, although soil pH decreased from 7.27 to 7.10 (Table 1). This is unsurprising because sulfate addition also increases soil As bioavailability through anion competition. Upon addition of a large amount of sulfate, competitive adsorption with As for binding sites results in the adsorption of some sulfate by the soil solid phase, along with As exchange into the soil solution (Goh and Lim, 2004). Therefore, the overall effect of sodium sulfate on rhizosphere soil As bioavailability is not significant. This result is consistent with the findings of Xu et al. (2019); namely, As mobilization in six of eight soils was not affected by the addition of sodium sulfate. Decreased As and Cd bioavailability to rice plants is a mechanism of sulfate-induced decrease in As and Cd concentrations in rice grain (Hu et al., 2007; Fan et al., 2010; Zhang et al., 2019). However, this mechanism does not work in wheat. As mentioned above, the mobilization of As and 11

Journal Pre-proof Cd in wheat rhizosphere soil were not decreased by sodium sulfate application. Notably, Cd mobilization was increased by sodium sulfate application, thereby increasing Cd accumulation in wheat root (Fig. 4). Similar to Cd, the root As concentration was increased by sodium sulfate application. However, the As and Cd concentrations in wheat grain and straw were decreased and unchanged, respectively, by sodium sulfate application (Fig. 4). These results suggest that the extents of of As and Cd translocation from wheat root to shoot and from straw to grain were decreased by the application of sodium sulfate, which led to lower As and Cd concentrations in wheat grain (Figs. 4 and 5). The decrease of As and Cd translocation caused by sodium sulfate application is potentially

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because sodium sulfate application increased the root and straw S concentrations (Fig. 8) and

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synthesis of S-containing ligands, such as glutathione and phytochelatins; notably, these ligands promote As and Cd sequestration into vacuoles by chelation, thereby decreasing As and Cd

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translocation. This hypothesis is supported by the findings of previous studies on rice (Liu et al.,

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2010b; Duan et al., 2011; Cao et al., 2018). Furthermore, the sodium sulfate-induced enhancement of

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P accumulation in wheat root and straw might explain the decreased translocation of As and Cd in wheat plants. Arsenic translocation in rice plants is inhibited by P (Wu et al., 2011), and the grain As

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concentration is negatively correlated with the straw P concentrations in rice and wheat (Norton et al., 2010; Shi et al., 2015). Phosphorous decreases Cd translocation in plants by binding Cd to the cell

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wall and forming insoluble Cd-phosphate complexes, such as Cd3(PO4)2 and CdHPO4 (Qiu et al., 2011). In addition to the decreased translocation of As and Cd, the sodium sulfate-induced increase in wheat grain weight may exert a dilution effect, thereby lowering the As and Cd concentrations in wheat grain.

As expected, sodium sulfate addition to soil increased S uptake. Moreover, sodium sulfate addition significantly increased N and P uptake by wheat (Fig. 7). Similarly, Jackson (2000) and Salvagiotti et al. (2009) reported that sulfate addition increased P and N uptake in canola and wheat, respectively. There are three possible mechanisms for these results. First, S fertilizer addition increased plant root biomass and root volume, enhancing N and P capture from soil (Katterer et al., 1993; Salvagiotti and Miralles, 2008). Second, in this study, the rhizosphere pH decreased from 7.27 to 7.10 after S application, resulting in a soil pH close to the ideal value (i.e., 6.5–6.8) for wheat N and P uptake (Sigua et al., 2016). Therefore, the decrease in soil pH after S application increased the solubility and uptake of N and P by wheat. Third, the increased S concentration in plant will increase 12

Journal Pre-proof plant N and P acquisition to match its protein concentration and the demand for ribosomal RNA synthesis (Prodhan et al., 2017).

5. Conclusions Sodium sulfate application decreased the wheat grain As and Cd concentrations and promoted the growth of wheat in As and Cd co-contaminated soil. The sodium sulfate-induced decreases of As and Cd concentrations in wheat grain were not caused by decreased As and Cd bioavailability in rhizosphere soil; however, these decreases were caused by diminished As and Cd translocation.

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Moreover, sodium sulfate application decreased lipid peroxidation and enhanced photosynthesis; it

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also increased N, P, and S uptake and enhanced the growth of wheat in As and Cd co-contaminated soil. The increased P and S concentrations in wheat root and straw might have contributed to the

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decrease of As and Cd translocation. Therefore, sulfate application in As and Cd co-contaminated

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agricultural soil may be an effective method for decrease of As and Cd accumulation in wheat grain

Acknowledgements

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and a means to decrease the risks of these substances to human health.

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This work was financially supported by the National Natural Science Foundation of China (41601541, 41601320, and 31671690), the Natural Science Foundation of Jiangsu Province

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(BK20160593 and BK20161375), Young Elite Scientists Sponsorship Program from the Jiangsu Association for Science and Technology, and the Jiangsu Provincial Government Scholarships for Overseas Investigation. The authors are grateful to Ms. Shiwei Xu and Ms. Chenye Yang for their technical assistance with inductively coupled plasma mass spectroscopy.

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Priority List of Hazardous Substances, the Subject of Toxicological Profiles. https://www.atsdr.cdc.gov/SPL/ (Accessed 2 September 2019). Avery, B.W., Bascomb, C.L., 1982. Soil survey laboratory methods. Harpenden, soil survey technical monograph no. 6. Harpenden, Hertfordshire: Rothamsted Experimental Station, UK. Bao, S.D., 2000. Soil and agricultural chemistry analysis. China Agriculture Press, Beijing (in Chinese). Beesley, L., Moreno-Jiménez, E., Gomez-Eyles, J.L., 2010. Effects of biochar and greenwaste compost amendments on mobility, bioavailability and toxicity of inorganic and organic contaminants in a multi-element polluted soil. Environ. Pollut. 158, 2282–2287. Bhattacharya, P., Samal, A.C., Majumdar, J., Santra, S.C., 2010. Accumulation of arsenic and its distribution in rice plant (Oryza sativa L.) in Gangetic West Bengal, India. Paddy Water Environ. 8, 63–70. Bolan, N.S., Adriano, C.C., Duraisamy, P., Mani, A., Arulmozhiselvan, K., 2003. Immobilization and phytoavailability of cadmium in variable charge soils. I. Effect of phosphate addition. Plant Soil 250, 83–94. Cao, Z.Z., Qin, M.L., Lin, X.Y., Zhu, Z.W., Chen, M.X., 2018. Sulfur supply reduces cadmium uptake and translocation in rice grains (Oryza sativa L.) by enhancing iron plaque formation, cadmium chelation and vacuolar sequestration. Environ. Pollut. 238, 76–84. Capaldi, F.R., Gratão, P.L., Reis, A.R., Lima, L.W., Azevedo, R.A., 2015. Sulfur metabolism and stress defense responses in plants. Trop. Plant Biol. 8, 60–73. Chi, Y., Li, F., Tam, N. F. Y., Liu, C., Ouyang, Y., Qi, X, Li WC, Ye, Z., 2018. Variations in grain cadmium and arsenic concentrations and screening for stable low-accumulating rice cultivars from multi-environment trials. Sci. Total. Environ. 643, 1314–1324. de Livera, J., McLaughlin, M.J., Hettiarachchi, G.M., Kirby, J.K., Beak, D.G., 2011. Cadmium solubility in paddy soils: Effects of soil oxidation, metal sulfides and competitive ions. Sci. Total. Environ. 409, 1489–1497. Dixit, G., Singh, A.P., Kumar, A., Singh, P.K., Kumai, S., Dwivedi, S., Trivedi, P.K., Pandey, V., Norton, G.J., Dhankher, O.P., Tripathi, R.D., 2015. Sulfur mediated reduction of arsenic toxicity involves efficient thiol metabolism and the antioxidant defense system in rice. J. Hazard. Mater. 298, 241–251. Dixit, S., Hering, J.G., 2003. Comparison of arsenic (V) and arsenic (III) sorption onto iron oxide minerals: implications for arsenic mobility. Environ. Sci. Technol. 37, 4182–4189. Duan, G., Shao, G., Tang, Z., Chen, H., Wang, B., Tang, Z, Yang Y, Liu Y, Zhao, F.J., 2017. Genotypic and environmental variations in grain cadmium and arsenic concentrations among a panel of high yielding rice cultivars. Rice 10, 9. Duan, G.L., Hu, Y., Liu, W., Kneer, R., Zhao, F., Zhu, Y., 2011. Evidence for a role of phytochelatins in regulating arsenic accumulation in rice grain. Environ. Exp. Bot. 71, 416–421. Duncan, E.G., Maher, W.A., Foster, S.D., Krikowa, F., O'Sullivan, C.A., Roper, M.M., 2017. Dimethylarsenate (DMA) exposure influences germination rates, arsenic uptake and arsenic species formation in wheat. Chemosphere 181: 44–54. Fan, J.L., Hu, Z.Y., Ziadi, N., Xia, X., Wu C.Y.H., 2010. Excessive sulfur supply reduces cadmium accumulation in brown rice (Oryza sativa L.). Environ. Pollut. 158, 409–415. FAO - Food and Agriculture Organization, 2019. FAO Cereal Supply and Demand Brief. http://www.fao.org/worldfoodsituation/csdb/en/ ( Accessed 11 September 2019). 14

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Journal Pre-proof Table and figure captions Table 1. Changes in soil pH and CaCl2-extractable As and Cd (mg kg−1) in rhizosphere soils of two wheat cultivars (JM85 and MM45) at maturity, grown in contaminated soils with sodium sulfate application at 0 (S0), 60 (S60), or 120 (S120) mg kg−1. Fig. 1. Grain (a), straw (b), and root (c) biomasses (dry weight) of two wheat cultivars (JM85 and MM45) grown in contaminated soils with sodium sulfate application at 0 (S0), 60 (S60), or 120 (S120) mg kg−1. Data are means ± standard deviations (n = 3). Letters above error bars denote

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significant differences (p ≤ 0.05) between sulfate treatments within each wheat cultivar. Fig. 2. Net photosynthetic rate (Pn), stomatal conductance (Gs), intercellular CO2 concentration (Ci),

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and transpiration rate (Tr) in the flag leaves of two wheat cultivars (JM85 and MM45) grown in

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contaminated soils with sodium sulfate application at 0 (S0), 60 (S60), or 120 (S120) mg kg−1. Data are means ± standard deviations (n = 3). Letters above error bars denote significant

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differences (p ≤ 0.05) between sulfate treatments within each wheat cultivar.

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Fig. 3. Malondialdehyde (MDA) concentrations in the flag leaves of two wheat cultivars (JM85 and MM45) grown in contaminated soils with sodium sulfate application at 0 (S0), 60 (S60), or 120

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(S120) mg kg−1. Data are means ± standard deviations (n = 3). Letters above error bars denote significant differences (p ≤ 0.05) between sulfate treatments within each wheat cultivar.

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Fig. 4. Concentrations of As and Cd in the grain (a, b), straw (c, d), and root (e, f) of two wheat cultivars (JM85 and MM45) grown in contaminated soils with sodium sulfate application at 0 (S0), 60 (S60), or 120 (S120) mg kg−1. Data are means ± standard deviations (n = 3). Letters above error bars denote significant differences (p ≤ 0.05) between sulfate treatments within each wheat cultivar. Fig. 5. Ratios of As concentrations among plant parts (a, b) and proportions of As in grain (c) and straw (d) of two wheat cultivars (JM85 and MM45) grown in contaminated soils with sodium sulfate application at 0 (S0), 60 (S60), or 120 (S120) mg kg−1. Data are means ± standard deviations (n = 3). Letters above error bars denote significant differences (p ≤ 0.05) between sulfate treatments within each wheat cultivar. Fig. 6. Ratios of Cd concentrations among plant parts (a, b) and proportions of Cd in grain (c) and straw (d) of two wheat cultivars (JM85 and MM45) grown in contaminated soils with sodium 20

Journal Pre-proof sulfate application at 0 (S0), 60 (S60), or 120 (S120) mg kg−1. Data are means ± standard deviations (n = 3). Letters above error bars denote significant differences (p ≤ 0.05) between sulfate treatments within each wheat cultivar. Fig. 7. Total N (a), P (b), and S (c) uptake by two wheat cultivars (JM85 and MM45) grown in contaminated soils with sodium sulfate application at 0 (S0), 60 (S60), or 120 (S120) mg kg−1. Data are means ± standard deviations (n = 3). Letters above error bars denote significant differences (p ≤ 0.05) between sulfate treatments within each wheat cultivar. Fig. 8. Concentrations of N, P, and S in grain (a, d, g), straw (b, e, h), and root (c, f, i) of two wheat

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cultivars (JM85 and MM45) grown in contaminated soils with sodium sulfate application at 0

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(S0), 60 (S60), or 120 (S120) mg kg−1. Data are means ± standard deviations (n = 3). Letters above error bars denote significant differences (p ≤ 0.05) between sulfate treatments within each

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wheat cultivar.

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Declaration of Competing Interest The authors declare that they have no known competing financial interest or personal

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relationships that could have appeared to influence the work reported in this paper.

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Table 1. Changes in soil pH and CaCl2-extractable As and Cd (mg kg−1) in rhizosphere soils of two wheat cultivars (JM85 and MM45) at maturity, grown in contaminated soils with sodium sulfate application at 0 (S0), 60 (S60), or 120 (S120) mg kg−1. CaCl2-Extractable As

CaCl2-Extractable Cd

S0

7.26 ± 0.07 a

0.66 ± 0.04 a

0.087 ± 0.003 b

S60

7.18 ± 0.06 ab

0.58 ± 0.08 a

0.093 ± 0.010 b

S120

7.09 ± 0.03 b

0.66 ± 0.11 a

0.116 ± 0.009 a

S0

7.28 ± 0.07 a

0.71 ± 0.04 a

S60

7.18 ± 0.08 ab

S120

7.11 ± 0.07 b

0.102 ± 0.011 b

0.65 ± 0.04 a

0.092 ± 0.018 b

0.66 ± 0.06 a

0.134 ± 0.012 a

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MM45

pH

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JM85

Treatment

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Cultivar

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Data are means ± standard deviations (n = 3). Letters in each data column indicate significant differences (p ≤ 0.05)

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between sulfate treatments within each wheat cultivar.

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Journal Pre-proof Highlights 

Sulfate application increased the growth and grain yield of wheat grown in As and Cd co-contaminated soil. Sulfate application did not reduce As and Cd bioavailability in wheat rhizosphere soil.

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Sulfate application increased As and Cd concentrations in root, but reduced them in grain.

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Sulfate application increased the uptake of N, P, and S by wheat plants.

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Sulfate application increased photosynthesis and reduced lipid peroxidation.

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