The threshold effect between the soil bioavailable molar Se:Cd ratio and the accumulation of Cd in corn (Zea mays L.) from natural Se-Cd rich soils

Science of the Total Environment 688 (2019) 1228–1235

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The threshold effect between the soil bioavailable molar Se:Cd ratio and the accumulation of Cd in corn (Zea mays L.) from natural Se-Cd rich soils Zezhou Zhang a, Linxi Yuan b,c,⁎, Shihua Qi a, Xuebin Yin d a

State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan, China Agricultural College of Yangzhou University, Yangzhou, China Jiangsu Bio-Engineering Research Centre of Selenium, Suzhou, China d Key Laboratory of Functional Agriculture, Suzhou Institute for Advanced Study, University of Science and Technology of China, Suzhou, China b c

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• Interactive effects were investigated on the translocation and uptake of Se and Cd from natural Se-Cd rich soils to crops. • A threshold effect between the soil bioavailable Se:Cd molar ratios (0.7) and the accumulation of Cd in corn. • Selenocystine could co-exist with Cd in the leaves in the lower soil bioavailable Se:Cd group (b 0.7). • Selenomethionine was bound to Cd in the leaves in the higher soil bioavailable Se:Cd group (N 0.7).

a r t i c l e

i n f o

Article history: Received 11 April 2019 Received in revised form 22 May 2019 Accepted 21 June 2019 Available online 22 June 2019 Editor: Xinbin Feng Keywords: Selenium (Se) Cadmium (Cd) Threshold effects Molar ratios Selenium speciations

a b s t r a c t There is little available information about the important interactions between selenium and cadmium (Se-Cd) in crops grown on natural Se-Cd rich soils. We investigated their interactive effects on the translocation and uptake of Se and Cd from soils to crops. Corn (Zea mays L.) roots, stems, leaves, and grains, and their corresponding rhizosphere soils were collected from naturally Se-Cd rich areas in Wumeng Mountain, Guizhou, China. The Se and Cd levels were determined in the soils, roots, stems, leaves, and grains. Soil bioavailable Se and Cd were also determined. The low soil bioavailable molar ratios for Se and Cd (Se:Cd) (≤0.7) improved Cd accumulation in the plants. However, relatively high Se:Cd molar ratios (N0.7) in the soils prevented Cd from entering the plants, but the effect of the soil Se:Cd on Se accumulation in corn was not significant. The strong anion exchange-high performance liquid chromatography-inductively coupled plasma mass spectroscopy (SAX-HPLC-ICP-MS) chromatograms showed that Se-Cd complexes occurred in the leaves, which likely indicated that direct interactions between Se and Cd happened there. The results suggested that thresholds for soil bioavailable Se:Cd molar ratios played a role in the interaction between Se and Cd in corn under natural conditions. © 2019 Elsevier B.V. All rights reserved.

1. Introduction ⁎ Corresponding author at: Jiangsu Bio-Engineering Research Centre of Selenium, Suzhou, China. E-mail address: [email protected] (L. Yuan).

https://doi.org/10.1016/j.scitotenv.2019.06.331 0048-9697/© 2019 Elsevier B.V. All rights reserved.

Cadmium (Cd) is a harmful heavy metal pollutant in soils and there is a risk of direct exposure to it via the food chain (Hamid et al., 2019).

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This has become an environmental concern due to its potential toxicity to humans and plants. It is assimilated via the gastrointestine and accumulates in the kidney where it becomes bound to metallothionein (MT). When the Cd levels in the body exceed the binding ability of MT, the Cd ions can give rise to hepato and nephrotoxicity (Rao et al., 2009), or increase free radical production and lipid peroxidation, which may inhibit hepatic and renal functions (Galazyn-Sidorczuk et al., 2009; Shi et al., 2019). The poisonous influence of Cd in plants has been previously investigated and the results showed that Cd can directly or indirectly cause oxidative damage to plants through the production of reactive oxygen species (Lin et al., 2012; Ansa et al., 2017; Bari et al., 2019). Cd could also affect plant metabolism and growth, leading to changes in enzymatic function, reduced seed yields, impaired photosynthesis, and membrane damage. It could also interfer with water and mineral nutrition (Shekhawat et al., 2010; Irfan et al., 2014). Therefore, plants have adopted various physiological defense strategies to avoid Cd phytotoxicity, such as phytochelation and sequestration (Filek et al., 2008; Pedrero et al., 2008; Lin et al., 2012). Glutathione (GSH), phytochelatins (PCs), and MT are important sulfurcontaining functional groups in plants and play an important role in plant Cd regulation as antagonists, antioxidants, or chelating agents (Zhu et al., 1999; Cobbett and Goldsbrough, 2002). Selenium (Se) shares similar chemical characteristics with sulfur, and selenols are even more reactive toward Cd than thiols (Tran et al., 2007; Zhou et al., 2009; Li et al., 2010; Pappas et al., 2011; Al-Waeli et al., 2012; Malik et al., 2012; Nahar et al., 2016). To date, antagonistic effects between Se and Cd have been observed in several plants (P.P. He et al., 2004; Ahmad et al., 2016; Sun et al., 2016; Wu et al., 2016) and animals (Jin et al., 2018; Abu-El-Zahab et al., 2019; Li et al., 2019). Sun et al. (2013) showed that exogenous Se significantly reduced Cd poisoning symptoms in corn (Zea mays L.) plants under hydroponic conditions, and the application of Se markedly reduced Cd accumulation in rice grains grown in Cd-contaminated soil (Hu et al., 2013). Other studies have shown that increasing Se levels alleviated Cd toxicity in rice (Lin et al., 2012), pepper (Mozafariyan et al., 2014), garlic (Sun et al., 2010), and sunflower (Saidi et al., 2014). However, these studies were conducted under laboratory-controlled conditions and further research should be carried out to explore Se and Cd interactions in natural Se-Cd rich soils. A geological survey in 2014 reported that the Cd and Se contents in soils from the Wumeng Mountain area, Guizhou, China reached 1.43–3.74 mg/kg and 0.35–1.04 mg/kg, respectively (S. He et al., 2004), which meant that this area was an ideal site to investigate the interactive effects between Cd and Se under natural conditions. The objectives of this study were as follows: 1) to investigate the characteristics of the bioavailable Se and Cd fractions in soils; 2) to explore the relationship between the bioavailable molar Se:Cd ratios in soils and the Se and Cd accumulation and translocation in corn plants (Zea mays L.); and 3) to develop a model that describes the interaction between Se and Cd in soil-plant systems. 2. Material and methods 2.1. Sampling Based on the geological survey data by the Geological Survey of Guizhou in 2014, four sub-study sites were selected in Wumeng Mountain area, Guizhou, China in September 2015 (Fig. S1). There were a low Se and low Cd soil site (LL) (26° 54′ 48.85″ N, 104° 07′ 4.92″ E), a low Se and high Cd soil site (LH) (26° 54′ 05.32″ N, 104° 07′ 38.42″ E), a high Se and low Cd soil site (HL) (26° 51′ 50.58″ N, 104° 10′ 30.60″ E), and a high Se and high Cd soil site (HH) (26° 53′ 27.54″ N, 104° 08′ 42.80″ E). One corn (Zea mays L.) plant sample and three corresponding rhizosphere soil samples were collected in each corn sampling point. Totally, there were four corn sampling points and 12 soil sampling points at each site, which was about 500 m2 in size. The samples were collected

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using wooden shovels, carefully wrapped in a plastic bag, and then immediately transported to the laboratory. In total, 16 corn plants samples and 48 soil samples were collected.

2.2. Sample preparation The soil samples were air dried and plant debris was removed. Then the samples were ground in a mortar to pass through a 100 mesh. The plant samples were separated into roots, stems, leaves, and grains, rinsed in deionized water, oven-dried at 55 °C, ground to pass through a 100-mesh using a grinder, and stored in an airtight plastic container at 25 °C.

2.3. Extraction of the bioavailable Se and Cd fractions in the soils The bioavailable Se and Cd fractions in the soil samples were extracted using AB-DTPA (McLaughlin et al., 2000; Dhillon et al., 2005; Shaheen et al., 2017; Rehman et al., 2018; Shaheen et al., 2018). Exactly 5 g of treated soil was shaken in 20 mL of 0.5 M NH4HCO3 and 0.005 M diethylenediamine pentaacetic acid (DTPA) for 2 h at 25 °C. The supernatant was collected as the bioavailable Se and Cd fractions after centrifuging at 3000 rpm for 20 min.

2.4. Total Se and Cd determination The soil and plant samples were duplicated and digested using 8 mL nitric acid and 2 mL perchloric acid in a digestion tube for 12 h at 25 °C. The digestion solution was heated to 210 °C until white fumes were observed and then evaporated to about 2 mL. After cooling, one of the duplicated samples was made up to a volume of 25 mL using deionized water, and the total Cd concentration was determined by Atomic Absorption Spectroscopy (AAS). The other duplicated sample was acidified by adding 5 mL 12 mol/kg HCl to reduce selenate to selenite, and made up to 25 mL with deionized water for the Se analysis by Hydride Generation Atomic Fluorescence Spectrometry (HG-AFS 9230), as described by Yuan et al. (2013). Bush Branch (GBW 07603-GSV-2, Se = 120 ± 20 μg/kg, Cd = 380 ± 40 μg/kg) and Chestnut Soil (GBW 07402-GSS2, Se = 160 ± 40 μg/kg, Cd = 710 ± 220 mg/kg) were used as the standard reference materials. The relative standard deviation (RSD) was b3%, and the standard reference materials ranged from 84% to 117% and from 81% to 109% for Se and Cd, respectively.

2.5. Selenium and cadmium species analysis in plant tissues Exactly 1 g of powdered lyophilized plant sample was placed into a 40 mL glass vial. It was then treated with protease XIV and protease cellulase, and incubated overnight at 37 °C. After hydrolysis, all the samples were extracted by methanol chloroform water three-phase extractant. Detailed method descriptions were given by Banuelos et al. (2011). Strong anion exchange-high performance liquid chromatography (A SHIMADZU LC-20AT equipped with Hamilton PRP-X100 column) combined with inductively coupled plasma mass spectroscopy (Thermo Fisher Series X2) (SAX-HPLC-ICPMS) was used to analyze the Se species in the aqueous extracts (Banuelos et al., 2015). The Se component amounts recovered from the aqueous extracts were determined by the area normalization method. The retention times for the 78Se and 111 Cd isotopes were monitored using ICP-MS and the sample retention times were directly compared to the following Se standards: selenocystine (SeCysCysSe), L-Se-methylseleno-cysteine (SeMeCys), selenomethionine (SeMet) (Tokyo Chemical Industry, Co., Japan), and 2− selenite (SeO2− 3 ) and selenate (SeO4 ) (National Reference Material Centre, China).

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2.6. Statistical analysis Microsoft Excel 2013 and SPSS 19 were used for the statistical analysis. The results are reported as the means ± standard deviation (SD). Correlation coefficients (R2), significance probabilities (p) and residual errors for linear regression fitting were calculated based on the scatter characteristics. The significant differences were analyzed by a oneway ANOVA performed by SPSS 19 (at a significance level of p = 0.05). 3. Results 3.1. Se and Cd levels in soils Total Se and Cd concentrations in the soil samples are shown in Fig. 1. The total Se concentrations in the 48 soil samples ranged from 533 to 962 μg/kg (DW) with mean and median values of 770 and 849 μg/kg (n = 48), respectively, which meant they were Se-rich soils (450–2000 μg/kg) according to Tan (1996). The total Cd concentrations ranged from 1565 to 2264 μg/kg, with a mean (median) value of 1900 (1870) μg/kg (n = 48). The Cd contents of all soil samples exceeded Class 2 limit values (1000 μg/kg) (Standardization Administration of the People's Republic of China, 2008) according to the Environmental Quality Standard for Soils in China, which meant that they were Cd polluted soils. Overall, the soils at the four subsites were classified as low Se/low Cd (LL), low Se/high Cd (LH), high Se/low Cd (HL), and high Se/high Cd (HH), which confirmed the 2014 geological survey data from the Geological Survey of Guizhou. The bioavailable Se and Cd concentrations in the soils are shown in Fig. S2. The highest bioavailability percentage for Se was observed in the LL group as 24.1 ± 3% (n = 12, pH = 7.1), but the lowest bioavailability percentage for Se was found in the HL group as 17.2 ± 1% (n = 12, pH = 5.2). In contrast, the highest bioavailability percentage for Cd was observed in the HL group as 25.9 ± 3%, and the lowest bioavailability percentage was in the LL group as 16.6 ± 4%. Overall, there were no differences on bioavailability percentages of Se in soils among LL, LH and HH, but significantly higher than those in HL. However, the bioavailability percentages of Cd in HL were significantly higher than those in LL, but no obvious differences among LL, LH and HH. These results could be explained that lower pH in HL (pH = 5.2) could promote Cd but inhibited Se to release as the bioavailable fractions (Li et al., 2017; Soltan et al., 2019). 3.2. Se and Cd levels in corn plant tissues The Se concentrations in the corn plant tissues were 179–232 μg/kg with a mean of 205 ± 28 μg/kg (n = 16) in the roots, 23–87 μg/kg with a mean of 58 ± 20 μg/kg (n = 16) in the stems, 86–166 μg/kg with a mean of 126 ± 21 μg/kg (n = 16) in the leaves, and 10–90 μg/kg with a mean of 38 ± 27 μg/kg (n = 16) in the grains (Fig. S3). The Cd concentrations in the leaves (2138 ± 1338 μg/kg, n = 16) were significantly higher

than in the roots (1428 ± 302 μg/kg, n = 16), stems (474 ± 268 μg/kg, n = 16), and grain (250 ± 87 μg/kg, n = 16) (p b 0.05) (Fig. S3). To study the relationship between the Se and Cd concentrations in corn plants, two exceptional values in Fig. 2a, b, c, d with the highest residual errors based on the residual error analysis were not included in this regression analysis, which were marked with red dots. We concluded that the molar concentrations for Se and Cd had a slightly negative relationship in the roots, stems, and grains (p N 0.05), but a significantly negative relationship in the leaves (p b 0.05) (Fig. 2). Moreover, there were no significant correlations between the bioavailable Se contents in the soils and the total Se contents in the plant tissues (Fig. S4-left). However, the Cd contents in the roots and stems significantly increased (R2 = 0.51, p b 0.05 and R2 = 0.32, p b 0.05, respectively) as the bioavailable Cd contents rose in the soils, but there were no significant correlations between the bioavailable Cd contents in the soils and the total Cd contents in the leaves and grains (Fig. S4-right). 3.3. Effects of Se on Cd uptake and translocation in corn plants Based on the residual error analysis, two exceptional values with the highest residual errors were observed from the fitted regression curve in each tissue (Fig. 3a, b, c, d) and, coincidently, they were from the same two sampling points, indicating that these points could be anomalous. Thus, those data from these two sampling points were excluded in the following regression analysis. Then we found that when the Se: Cd molar ratios in the bioavailable soils were lower than 0.7, significant positive correlations were observed between the Se:Cd molar ratios in the bioavailable fractions of the soils and the Cd molar concentrations in the roots (R2 = 0.34, p b 0.05) and stems (R2 = 0.40, p b 0.05), but slight positive trends in the leaves (R2 = 0.20, p N 0.05) and grains (R2 = 0.13, p N 0.05). However, when the Se:Cd molar ratios in the bioavailable fractions of the soils were higher than 0.7, antagonistic Se effects on Cd uptake were observed in the roots (R2 = 0.67, p b 0.05), stems (R2 = 0.63, p b 0.05), leaves (R2 = 0.51, p N 0.05), and grains (R2 = 0.36, p N 0.05) (Fig. 3a, b, c, d). These results suggested that the lower soil molar Se:Cd bioavailable ratios (0.4–0.7) could enhance Cd accumulation in corn plants, especially in the roots and stems, but higher bioavailable Se levels in the soils could decrease Cd accumulation, especially in the roots and stems at high molar Se:Cd ratios (0.7–1.1). The translocation factor (TF) for Cd (i.e., TF-Cd(root-Cd/bioavailable-soil-Cd) = Cd concentrationroot/Cd concentrationbioavailable-soil) was used to show how efficient Cd translocation among soil, root, stem, leaf and grain. The TFs-Cd (root/bioavailable soil) significantly increased as the soil bioavailable Se:Cd molar ratios increased (R2 = 0.78, p b 0.01) (Fig. 3e), and a slight positive trend was observed between the soil bioavailable Se:Cd molar ratios and the TFs-Cd (leaf/stem) (R2 = 0.24, p N 0.05) (Fig. 3g). However, there was a negative relationship between the soil bioavailable Se:Cd molar ratios and the TFs-Cd (grain/leaf) (R2 = 0.24, p N 0.05) (Fig. 3h). There were no threshold effects in Fig. 3e, g and h, which were quite different with Fig. 3a, c and d. But a threshold effect occurred between the TFs-Cd (stem/root) and the soil bioavailable Se:Cd molar ratio, although it was not significant (p N 0.05) (Fig. 3f). These results suggested that the elevated molar Se:Cd ratios in soils could significantly improve the translocation of Cd from the soil to the root, and then from the stem to the leaf. However, translocation from the leaf to the grain slightly decreased. The lower soil Se:Cd ratios (0.4–0.7) slightly enhanced Cd translocation from the root to the stem, but higher molar Se:Cd ratios (0.7–1.1) slightly decreased Cd translocation to the stems. 3.4. Effects of Cd on Se uptake and translocation in corn plants

Fig. 1. Selenium and cadmium levels and distributions in soils.

Overall, the effects of the soil bioavailable molar ratio (Se:Cd) on Se concentrations and TFs-Se values in the different tissues were not significant (p N 0.05) (Fig. 4). However, there were threshold effects between Se concentrations in the roots and stems, the TFs-Se (root/bioavailable soil) and TFs-Se (stem/root), and soil bioavailable molar ratios (Se:

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Fig. 2. Relationships between Se and Cd molar concentrations (μmol/kg) in roots (a), stems (b), leaves (c) and grains (d). The two “exceptional values” indicated as red dots were not included in the regression analysis. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 3. Relationships between the Cd concentrations and the soil bioavailable molar ratios for Se:Cd in different corn tissues: (a) roots, (b) stems, (c) leaves, and (d) grains. Soil bioavailable molar ratios for Se:Cd were compared with the TFs for Cd in different parts of the corn plants: (e) TFs for Cd (root/bioavailable soil), (f) TFs for Cd (stem/root), (g) TFs for Cd (leaf/stem), and (h) TFs for Cd (grain/leaf). The two “anomalous sampling points” indicated as red dots were not included in the regression analysis. All correlation coefficients were estimated by linear regression. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

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Fig. 4. Relationships between the Se concentrations and soil bioavailable Se:Cd molar ratios in the corn tissues: (a) roots, (b) stems, (c) leaves, and (d) grains. Soil bioavailable molar ratios for Se:Cd were compared with the TFs for Cd in different parts of the corn plants: (e) TFs for Se (root/bioavailable soil), (f) TFs for Se (stem/root), (g) TFs for Se (leaf/stem), and (h) TFs for Se (grain/leaf). The two “anomalous sampling points” were not included in the regression analysis. All correlation coefficients were estimated by linear regression.

Cd), respectively (Fig. 4a, b, e, f). Especially, the TFs-Se (root/bioavailable soil) were significantly positively related to the soil bioavailable molar ratios (Se:Cd) (R2 = 0.60, p b 0.05) when the molar ratios were higher than 0.7 (Fig. 4e). Furthermore, the variation trends for the Se accumulation characteristics (Fig. 4a, b, c, d) were similar with those for TFs-Se in the different plant tissues (Fig. 4e, f, g, h). 4. Discussion Se alleviation of heavy metal toxicity in plants by decreasing the uptake of heavy metals has been previously reported (Ebbs and Weinstein, 2001; P.P. He et al., 2004; Zhang et al., 2012; Shekari et al., 2019). Furthermore, Se biofortification strategies have been shown to alleviate growth inhibition induced by heavy metals (Filek et al., 2008; Zembala et al., 2010; Feng et al., 2013a). Qutab et al. (2017) reported that Se in the root zone mitigated Cd-induced decreases in total proteins in the roots of corn (Zea mays L.) under different Cd regimes, and Lin et al. (2012) found that exogenous Se significantly decreased Cd concentrations and alleviated oxidative stress in rice. Selenium often exerts a dual effect on the uptake and translocation of heavy metals in plants, which are both dependent on the concentrations of bioavailable forms of Se and heavy metals in soils (Feng et al., 2013b; Ding et al., 2014; Saidi et al., 2014; Qing et al., 2015; Yu et al., 2018). However, there is little available information about the threshold effects between soil bioavailable molar Se: Cd and the uptake and translocation of Cd and Se in staple crops. To

date, only a few studies have investigated the molar interaction between Se and Hg. Wang et al. (2016) found that Hg-Se nanoparticles existed in Se-amended soils at a molar ratio of 1:1, and Zhang et al. (2012) have shown that the formation of covalent Hg-Se insoluble bonds (1:1 M ratio of Hg:Se) between the soil and roots reduced the bioavailable Hg contents in rhizosphere soils. MacDonald et al. (2015) have shown that endogenous Se can sequester inorganic Hg as an insoluble mixed chalcogenide, HgSxSe(1−x) (x can be 0.4–0.9). Therefore, this study is the first to report on a threshold effect between the soil bioavailable molar Se:Cd ratios and the accumulation and translocation of Cd in corn. Huang et al. (2018) suggested that Se in the soil may thermodynamically react with Cd to form Cd-Se complexes, which are not bioavailable to the plant roots and results in the inhibition of Cd uptake and xylem translocation to the aerial part. Higher plants metabolize Se forms via sulfur-assimilation pathways (Zhu et al., 2009), and relatively abundant Se levels can be more easily reduced to selenides by higher plants, which are then incorporated into amino acids and proteins (PilonSmits et al., 1999). The Cd within cells is often bound to sulfur ligands, especially thiol groups, such as GSH and PCs (Huang et al., 2017; Yu et al., 2017), and more active to –SeH, such as SeCys, GSH-PCs (Yadav, 2010). The possible mechanisms underlying the uptake and translocation of Cd and Se in corn are proposed to be as follows (Fig. 6): (1) Root to soil: When the soil bioavailable Se:Cd molar ratio was lower than 0.7, significant positive correlations were observed

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between the soil bioavailable Se:Cd molar ratios and the Cd molar concentrations in the roots (Fig. 3a). The Se and Cd are probably transported into the roots as CdSeO03 and CdSeO04, which are taken up more efficiently (Yu et al., 2018). However, when the soil bioavailable Se:Cd molar ratios are higher than 0.7, Se-Cd complexation can occur via Se reduction in an acid soil environment (SeO2− → SeO23 → Se0 → Se2−) (Shanker 4 et al., 1996). These complexes are not bioavailable to plant roots, which means that there is a significant decrease on Cd accumulation in the roots (Fig. 3a) and a significant increase in TFsCd (root/bioavailable soil) (Fig. 3e). Furthermore, Se increases the lignin contents and thickness of cell walls by regulating the expression of Cd-related and lignin synthesis genes, which improves the mechanical strength of the cell walls and decreases Cd diffusion into plant cells (Cui et al., 2018). There were no obvious co-existence peaks between Se and Cd in roots after SAXHPLC-ICP-MS analysis (Fig. 5a, b), suggesting that the interactive effects may happen in the soils rather than in the roots. (2) Root to stem: The variation trends were almost the same for the accumulation and transportation of Se and Cd in stems (Figs. 3b, f, 4b, f), which suggested that the stem was just a transport tissue and there was no Se-Cd interaction there. (3) Stem to leaf: In the leaves, Cd-selenol complexes (such as GSH, PCs, and complex formation between Cd and seleno-amino acids) are mostly stored in the vacuole where they cannot cause further damage to tissue cells (Clemens, 2006; Ernst et al., 2008). The SAX-HPLC-ICP-MS analysis revealed that SeCysCysSe could co-exist with Cd in the leaves of plants from the lower Se:Cd group (b0.7) (Fig. 5c), but SeMet was bound to Cd in the plants from the higher Se:Cd group (N0.7) (Fig. 5d).

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(4) Leaf to grain: There were no significant correlations between the TFs for Se, the Se accumulation characteristics, and the molar ratios Se:Cd in soils (Fig. 4d, h). This might be due to a special protective mechanism in grain because it is an energy storage and reproductive tissue. We identified that there was a threshold effect between the soil bioavailable Se:Cd molar ratios and the accumulation and translocation of Cd in corn (Zea mays L.) grown in natural Se-Cd rich soils. When the soil bioavailable Se:Cd molar ratios were higher than 0.7, the increased levels of bioavailable Se in the soil could significantly decrease Cd accumulation in corn plants. Higher Se levels also significantly increased the TFs-Cd from soil to root, but decreased translocation from the root to the aerial part. In China, about 7% of the soils are polluted by Cd and about 10% of rice samples contain excessive amounts of Cd (Zhang et al., 2015). Our findings showed that soil Cd pollution could be remediated by adding Se fertilizer to the soil to restrict Cd transportation into the roots and edible parts of staple crops. Furthermore, we have a Se deficiency zone in China and 39–61% population suffer from Se deficiency because Se intake is lower than the Se dietary intakes recommended by WHO/FAO (26–34 μg/day/adult) (Ullah et al., 2018). Many natural Se soil resources are being utilized to produce Se-rich agricultural products (Wu et al., 2015), but Se is usually accompanied by Cd in natural Serich soils, which causes a potential health risk to persons consuming naturally Se-rich agriculture products (Du et al., 2018; Yang et al., 2019). This study revealed that natural Se in soils should be activated to reduce Cd accumulation in staple crops. Furthermore, the coexistence of Se-Cd species in leaves shown in this study could improve our understanding about the interaction between Se and Cd in staple crops, which could affect the toxicity of Cd in crops.

Fig. 5. Typical chromatographic separation and identification spectrograms on the soluble Se and Cd compounds present in the roots and leaves after protease XIV digestion using strong anion exchange high pressure liquid chromatographic inductively coupled mass spectrometry (SAX-HPLC-ICPMS). (a) Selenium-containing peaks, monitored as 78Se, and cadmiumcontaining peaks, monitored as 111Cd, appear in root when the soil bioavailable fraction molar ratios for Se:Cd ≤ 0.7; (b) root peaks when the soil bioavailable fraction molar ratios for Se:Cd N 0.7; (c) leaf peaks when the soil bioavailable fraction molar ratios for Se:Cd ≤ 0.7; and (d) leaf peaks when the soil bioavailable fraction molar ratios for Se:Cd N 0.7.

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Fig. 6. Possible mechanism for the interaction between Se and Cd in soil-plant system.

Acknowledgments This work was supported by the Guangxi Innovation Special Project (GKAA17202026, GKAA17202038-1, GKAA2017AA19044, GKAA17202044-1, GKAA17202019-2, GKAA17202027-3), the Science and Technology Bureau of Enshi Tujia and Miao Autonomous Prefecture (XYJ2018000080), the National Natural Science Foundation of China (31400091), and the Natural Biofortification Program (NBP) by the International Society for Selenium Research (ISSR). The authors appreciated Prof. Shaolin He, Dr. Chunhu Mo and Dr. Wei Meng at Guizhou Geological Survey, Guiyang, China for helping samples collection. We also thank two anonymous reviewers for their valuable critical comments in improving the manuscript. Thanks to Associate Editor Prof Xinbin Feng for his carful edition. We also thank International Science Editing (http://www.internationalscienceediting.com) for editing this manuscript. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi. org/10.1016/j.scitotenv.2019.06.331. References Abu-El-Zahab, H.S.H., Hamza, R.Z., Montaser, M.M., El-Mahdi, M.M., Al-Harthi, W.A., 2019. Antioxidant, antiapoptotic, antigenotoxic, and hepatic ameliorative effects of L-carnitine and selenium on cadmium-induced hepatotoxicity and alterations in liver cell structure in male mice. Ecotoxicol. Environ. Saf. 173, 419–428. Ahmad, P., Abd, A.E.F., Hashem, A., Sarwat, M., Gucel, S., 2016. Exogenous application of selenium mitigates cadmium toxicity in Brassica juncea L. (Czern & Cross) by upregulating antioxidative system and secondary metabolites. J. Plant Growth Regul. 35, 936–950. Al-Waeli, A., Pappas, A.C., Zoidis, E., Georgiou, C.A., Fegeros, K., Zervas, G., 2012. The role of selenium in cadmium toxicity: interactions with essential and toxic elements. Br. Poult. Sci. 53, 817–827. Ansa, A.A., Akpere, O., Imasuen, J.A., 2017. Semen traits, testicular morphometry and histopathology of cadmium-exposed rabbit bucks administered methanolic extract of Phoenix dactylifera fruit. Acta Sci. Anim. Sci. 39, 207–215. Banuelos, G.S., Fakra, S.C., Walse, S.S., Marcus, M.A., Yang, S.I., Pickering, I.J., Pilon-Smits, E.A.H., Freeman, J.L., 2011. Selenium accumulation, distribution, and speciation in spineless prickly pear cactus: a drought- and salt-tolerant, selenium-enriched nutraceutical fruit crop for biofortified foods. Plant Physiol. 155, 315–327. Banuelos, G.S., Arroyo, I., Pickering, I.J., Yang, S.I., Freeman, J.L., 2015. Selenium biofortification of broccoli and carrots grown in soil amended with Se-enriched hyperaccumulator Stanleya pinnata. Food Chem. 166, 603–608. Bari, M.A., Akther, M.S., Abu, R.M., Kabir, A.H., 2019. Cadmium tolerance is associated with the root-driven coordination of cadmium sequestration, iron regulation, and ROS scavenging in rice. Plant Physiol. Biochem. 136, 22–33.

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