Selenium Application Decreases the Enrichment and Human Exposure Risk of Cadmium in the Leaf of Jute (Corchorus capsularis L.) Planted in Uncontaminated Purple Soil

Abstract

The effects of soil selenium (Se) application on the enrichment and human exposure risk of heavy metals in the jute (Corchorus capsularis L.) leaf have attracted extensive attention. The jute was planted with or without soil Se addition for 265 days. The jute leaf was harvested seven times during the experiment to determine the content of lead (Pb), cadmium (Cd), and Se. The results showed that the enrichment ability ranked Cd > Se > Pb. Cd in the jute leaf exceeded the average pollutant limit in GB2762-2017 by 1.37 times without Se application. The Se application is conducive to an increase of Se by 88.11–202.79%, contrarily reducing Cd by 35.40–38.32% and Pb by 9.58–26.57%. In general, the risk quotients (HQ) of Cd and Pb were decreased and less than 1 with Se treatment. Thus, the human exposure risk of Cd and Pb is negligible when ingesting the jute leaf via diet. It is suggested that Se can be applied to inhibit the enrichment of Cd and Pb in the jute production process to reduce the potential exposure risk of Cd and Pb to the human body and increase economic and nutritional values by raising Se levels in the jute leaf.

1. Introduction

With the development of the economy and industry, the cumulation of soil lead (Pb) and cadmium (Cd) was found in farmland, which has not only a particular impact on the safety of the farmland ecosystem but also human health [1,2]. Recovering and reusing polluted soil and taking effective measures to alleviate the enrichment and toxicity of soil heavy metals in crops is a tricky problem that needs to be solved urgently [3].

There are two main ideas for alleviating heavy metals enrichment in crops. The first idea is a conventional strategy for the phytoremediation of soil pollution [4]. Plants with large biomass, high economic value, and a specific heavy metal enrichment capacity, such as Azollapinnata and Arabispaniculata for Cd, were screened for phytoremediation due to their advantages of low cost, high efficiency, and environmental friendliness [5]. However, the economic value of agricultural products decreases significantly because of a potential health risk caused by a large number of heavy metals enrichment [6]. The second idea is just the opposite, that is, to take effective ways to restrict the enrichment of harmful heavy metals while increasing the accumulation of beneficial elements to obtain agricultural products with higher economic value [7], which has also become a new way worth exploring for the remediation of heavy metal polluted soil in the future [8].

Selenium (Se) is a beneficial element for crop growth. Applying Se to soil can speed up crop growth and increase crop yield and quality [9]. Studies have shown that foliar spraying of Se fertilizer can increase the Se content of rice grains and significantly reduce the content of harmful heavy metals such as copper, mercury, and Cd in rice [10]. The coprecipitation of Se and heavy metals in soil is crucial in reducing the absorption of heavy metals by plants. Soil pH, Eh, water, and microorganisms affect the ability of Se to reduce the absorption of heavy metals by changing the root morphology [11,12]. The latest research also showed that Se has the detoxification effect of heavy metals in the soil–plant–human body system, but it may have a double-edged sword effect [13,14].

The jute (Corchorus capsularis L.) is an annual subshrub herb with a fast growth speed and short maturity period. The jute leaf is characteristic of Se enrichment, high dietary fiber, and high calcium [15]. The jute leaf can be picked repeatedly throughout the growth duration [16]. The jute also has a specific adsorption and enrichment capacity for Pb, Zn, Cd, and Cr in soil and water [17]. Moreover, it was found that the distribution of Cd and Pb in jute during harvest is greater in roots than in leaves [18]. However, there are few reports on the effect of soil Se application on the enrichment of heavy metals such as Pb and Cd and their human exposure risk in the jute leaves via the diet pathway.

The jute planting experiment was carried out for 265 days. The soil was treated with Se, and the jute leaves were collected seven times. The contents of Pb, Cd, and Se were measured, respectively. The enrichment coefficient and hazard quotient (HQ) were assessed to verify the effects of soil Se application on the enrichment and human health risks of Pb and Cd in the jute leaves and provide reasonable suggestions for jute production in the purple soil region.

2. Materials and Methods

2.1. Soil

The farmland soil was collected from Longbao village, Wanzhou District, Chongqing in China, in February 2020. About 2 tons of topsoil (0–30 cm) were collected from about 1 acre of reclaimed paddy fields. The soil is mixed manually before storage. After air-drying, plant residuals and gravel were removed by passing a 5 mm sieve. The soil pH was 5.63, the Pb content was 24.4 mg/kg, and the Cd content was 0.21 mg/kg, which is lower than the GB 15618-2018 for the control of soil pollution risks in agricultural land. Thus, the soil is low-risk (

Table 1. Soil characteristics.

Classification	OM g/kg	TN g/kg	TP %	TK g/kg	NH4+-N%	NO3−-N %	pH	Pb mg/kg	Cd mg/kg	Se mg/kg
Purple soil	9.95	0.64	0.0569	18.4	0.30	0.064	5.63	24.4	0.21	0.22

).

2.2. Planting and Harvesting

The 10–20 jute seeds (Yucaima No.1, Chongqing southeast Academy of Agricultural Sciences) were directly planted in a flowerpot (36 cm × 36 cm) with 5 kg of soil. The field management was carried out, namely regular fertilization, watering, and insect repellent. Four seedlings were left when 3–4 true leaves sprouted. Seaweed concentrated nutrient solution was used as fertilizer, which mainly contains macroelements > 30 g/L, middle elements > 1 g/L, and microelements > 0.2 g/L, and no Cd and Pb were detected in the nutrient solution. The nutrient solution was mainly used to correct the nutrient deficiency and regulate plant growth. The ratio of nutrient solution to water was 1:400, which was poured on the roots of plants at the seedling stage. Deionized water was used in the whole planting process, and pesticides were not used. Therefore, theoretically, no other sources of heavy metals enter the soil–plant system. The jute leaf was harvested seven times in 110–265 days after sowing. After each harvest, the jute leaf was immediately killed in a 105 °C oven for 30 min and continued to dry at 80 °C until constant weight. The samples were stored in a dryer to determine Se, Cd, and Pb content.

2.3. Se Addition

According to the sensitivity of the jute to Se and the control value of soil pollution risk of agricultural land standard for soil pollution risk management and control of agricultural land (Trial) (GB 15618-2018), sodium selenite (Na₂SeO₃, chemically pure, Sinopharm Chemical Reagent Co., Ltd., Shanghai, China) of 0 mg/kg, 0.2 mg/kg, and 0.5 mg/kg (CK + 0Se, Ck + 1Se, and CK + 2Se) was added to the soil surface in powder one week before sowing.

2.4. Analysis Method

Soil organic matter and pH were determined by the standard of NY/T 1121.6-2006. Total nitrogen was analyzed by the standard of NY/T 1228-2015. Soil total phosphorus was determined by the alkali fusion-molybdenum antimony anti-spectrophotometric method (HJ632-2011). The total potassium was determined by the standard of NY/T 87-1988. The ammonium nitrogen and nitrate nitrogen were determined by the standard of NY/T 1116-2014. The Pb, Cd, and Se content in soil and plant was determined by an inductively coupled plasma emission spectrometer (ICP-MS, Agilent 7500) according to the standard of HJ 803-2016 and GB 5009.268-2016.

2.5. Calculation

The content of Pb, Cd, and Se in the jute leaf was calculated based on the fresh weight according to the standard of GB2762-2017 for food safety, as follows:

C_fresh = C_dry × m/M

(1)

where m is the dry weight of the sample (g), M is the fresh weight of the sample (g), C_dry is the heavy metal content calculated based on the dry weight (mg/kg), and C_fresh is the heavy metal content calculated based on the fresh weight (mg/kg).

The enrichment coefficient of heavy metals was calculated according to [19].

A_b = C_fresh/C_s

(2)

where A_b is the enrichment coefficient of heavy metals from soil to jute leaf; C_s is the concentration of heavy metals in soil, mg/kg; and C_fresh is the heavy metal content calculated based on the fresh weight (mg/kg).

The Monte-Carlo model was used to simulate the risk of human exposure to Cd and Pb pollution in the crop–soil system, and the calculation formula is as follows [20]:

CDI = C_s × A_b × IR_i × EF × ED/(365 × BW × AT)

(3)

HQ = CDI/RfD

(4)

where CDI is the daily intake of heavy metals per unit of body weight via diet, mg/(d·kg); C_s is the concentration of heavy metals in soil, mg/kg; A_b is the conversion coefficient of heavy metals from soil to jute leaf (enrichment coefficient). IR_i is the average daily exposure of the human body to a given crop via diet, kg/d, obtained from the national food intake data [21]. EF is the exposure frequency, d/a, and the default value is 350 d; ED is the exposure duration, a, and the default value is 70 a; BW is the average weight of middle-aged people (60.1 ± 10.9) kg; AT is the average life span, 76.72 a [22]. HQ is hazard quotient. RfD is the reference dose formulated by USEPA, 0.001 mg/kg for Cd and 0.004 mg/kg for Pb. HQ < 1 indicates that the soil pollution of heavy metals does not pose a health risk to the human body. HQ > 1 indicates that the soil pollution of heavy metals will cause health risks to the human body.

2.6. Statistics and Analysis

All data were collected with Excel 2010 and analyzed by SPSS 19.0. OriginPro 8.0 was used to plot the data. Each treatment had four replicates, and each sample was determined three times.

3. Results

3.1. Dynamic of Pb, Cd, and Se in the Jute Leaf

The contents of Pb, Cd, and Se in the jute leaf decreased first and then stabilized with time prolonged, and the contents of Pb and Cd in treatments of CK + 1Se and CK + 2Se were significantly lower than the control (CK + 0Se). Moreover, the content of Se in the jute leaf was shown as CK + 2Se > CK + 1Se > CK + 0Se (Figure 1).

3.2. Pb, Cd, and Se across Seven Harvest

Across seven harvests, with the Se application increase, the Pb content decreased by 9.58–26.57%, while the Se content increased by 88.11–202.79%. Furthermore, the Cd content exceeded the pollutant limit (0.2 mg/kg) by 1.37 times under control according to the national food safety standard of GB 2762-2017, while Se treatment reduced the average Cd content by 35.40% under CK + 1Se and 38.32% under CK + 2Se, respectively, so that it was lower than the pollutant limit of GB2762-2017 (Figure 2).

3.3. Enrichment Coefficient of Pb, Cd, and Se

The Se enrichment coefficient of the jute leaf increased from 0.068 to 0.204 with an average increase of 1.88–2.97 times, and the Cd enrichment coefficient decreased from 1.296 to 0.837 with an average decrease of 1.62 times, while the Pb enrichment coefficient was almost not changed from the data of the seven harvests. In general, the enrichment coefficient of heavy metals in the jute leaf was ranked as Cd > Se > Pb (Figure 3). It can be seen that the jute leaf has the strongest ability to enrich Cd, followed by Se.

3.4. Exposure Risk of Pb and Cd Enrichment

The content of Pb and Cd ingested by the human body through diet is related to the enrichment ability of the jute leaf to Pb and Cd and the level of Pb and Cd in soil. This study assumes that cooking does not affect the content of Pb and Cd in the jute leaf, that is, the content of Pb and Cd in the jute leaf is equal to the human intake.

4. Discussion

Se application is beneficial in reducing the enrichment level of Cd and Pb in the jute leaf. Studies showed that rice seedlings slightly increased the absorption of Cd in a short Se exposure while reducing the absorption and transport of Cd in a longer Se exposure [23]. The investigation of Se application in rice fields found that the Se application of 120 kg/hm² reduced the accumulation of Cd in rice panicles by 53% and 45%, respectively, but had no significant inhibitory effect on Pb [24]. Se can effectively reduce the transfer of Cd from root to shoot in rice seedlings [23]; Se can reduce the accumulation of Cd in seeds by increasing the retention of Cd in the roots of Brassica napus L. [25]; Se reduces Cd uptake by rice suspension cells by regulating lignin synthesis and the expression of Cd-related genes [26]. Se can promote plant growth and photosynthesis by regulating the absorption and transport of trace elements and reduce oxidative stress by mediating reactive oxygen species, so as to protect plants from toxic trace elements. The research review shows that the complexation of Se with toxic trace elements in the rhizosphere may help to reduce the absorption of these elements by plants [27]. Therefore, Se application is beneficial in reducing the enrichment of Pb and Cd in the jute leaf.

Se enrichment capacity and level of crops are closely related to soil Se addition and crop varieties. The pot experiment of eggplant seedlings found that when the amount of Se applied was 0–100 mg/kg, the Se content of eggplant roots was positively correlated with soil Se amount, and Se in the jute leaf first increased and then decreased with the increase of Se application [28]. It was found that when the concentration of exogenous Se was 10 mg/kg, the growth of watercress was the best [29]. Studies have also shown that Se application with 0–100 g/ha in rice leaf can increase the Se content of rice plants by 6.5–56 times [30].

The heavy metal enrichment coefficient refers to the ratio of the content of heavy metals in the edible part of crops to the content of heavy metals in the planting soil. It can reflect the absorption capacity of agricultural products to heavy metals under the same level of heavy metals in the soil. The greater the enrichment coefficient, the stronger the ability of crops to absorb certain heavy metals, and the more vulnerable they are to the impact of soil heavy metal pollution [31]. Based on the average content of Pb and Cd in edible jute leaf, the HQ of Pb and Cd in the jute leaf calculated by Equation (4) is less than 1 under the three Se treatments in

Table 2. Potential exposure risk via diet pathway.

Items	Elements	Treatments
		CK + 0Se	CK + 1Se	CK + 2Se
IRi		0.082	0.082	0.082
CDI	Pb	0.00014	0.00013	0.00010
	Cd	0.00033	0.00021	0.00020
	Se	0.00002	0.00003	0.00006
HQ	Pb	0.14	0.13	0.10
	Cd	0.33	0.21	0.20
	Se	0.02	0.03	0.06

. Thus, the exposure risk of Pb and Cd is small, and there is no health risk to the human body from eating the jute leaf. In addition, at a higher Se addition level, HQ of Pb is substantially lower, so it is more conducive to improving the quality of jute leaf and human health, even in unpolluted soil.

5. Conclusions

After growing for 265 days, the average Cd content in the jute leaf was 1.37 times higher than the limit of pollutants in food in the national food safety standard of GB 2762-2017 without Se application across seven harvests. The application of Se in the soil is conducive to reducing the enrichment of Pb and Cd in the jute leaf, resulting in an average Cd decrease by 35.40–38.32%, an average Pb decrease by 9.58–26.57%, and an average Se increase by 88.11–202.79%. The jute leaf has the strongest enrichment ability of Cd, followed by Se. The Se enrichment capacity and level of crops are closely related to the amount of Se added to the soil. In general, the HQ of Pb and Cd in the jute leaf under Se treatment is less than 1, and the exposure risk is negligible. It is suggested that Se should be added to the soil to inhibit the enrichment of Cd and Pb in the jute leaf, so as to reduce the potential exposure risk of heavy metals to the human body and increase the Se level.