Next Article in Journal
Examining Environmental Turbulence Intensity: A Strategic Agility and Innovativeness Approach on Firm Performance in Environmental Turbulence Situations
Previous Article in Journal
Artificial Intelligence-Enabled Game-Based Learning and Quality of Experience: A Novel and Secure Framework (B-AIQoE)
Previous Article in Special Issue
Alginate-Based Sustainable Green Composites of Polymer and Reusable Birm for Mitigation of Malachite Green Dye: Characterization and Application for Water Decontamination
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Sustainability
Volume 15
Issue 6
10.3390/su15065361
sustainability-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Reducing Chromium Toxicity in Chinese Cabbage through Synergistic Effects of Silicon and Selenium: A Study of Plant Growth, Chromium Content, and Biochemical Parameters

by
Xiuxian Fu
1,2,†,
Sajid Mehmood
1,2,†,
Waqas Ahmed
1,2,
Wenjie Ou
1,2,
Penghui Suo
1,2,
Qinwen Zhang
1,2,
Xiuhao Fu
1,2,
Zhongyi Sun
1,2,* and
Weidong Li
1,2,*
1
Center for Eco-Environment Restoration Engineering of Hainan Province, School of Ecological and Environmental Sciences, Hainan University, Haikou 570228, China
2
College of Ecology and Environment, Hainan University, Haikou 570100, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Sustainability 2023, 15(6), 5361; https://doi.org/10.3390/su15065361
Submission received: 5 February 2023 / Revised: 13 March 2023 / Accepted: 14 March 2023 / Published: 17 March 2023
(This article belongs to the Special Issue Sustainable Approaches for Plant Conservation under Emerging Pollutants Volume II)
Browse Figures
Review Reports Versions Notes

Abstract

:
Silicon (Si) and selenium (Se) have been found to reduce chromium (Cr) toxicity in plants, which is important for crop production and human health. However, there is limited understanding of the interaction between Si and Se in mitigating Cr toxicity and its mechanisms. This study investigated the impact of Si and Se on Cr-treated Chinese cabbage growth, Cr content, and biochemical parameters in a hydroponic experiment. The results showed that both Si and Se effectively alleviate Cr toxicity and have a strong synergistic effect. They reduced Cr content in cabbage by 73.99% and increased photosynthetic pigments by 62.50% and 47.51%, respectively. Antioxidant enzyme activity increased by 28.20 and 21.37%, while non-enzyme antioxidants such as proline and GSH decreased by 27.44 and 28.51%. It was observed that the addition of Si and Se to Chinese cabbage under Cr stress resulted in a 29.58 and 134.37% increase in soluble protein and soluble sugar, respectively, as well as improved nutrient contents (N, P, K, Ca, and Mg). This suggests that Si and Se can improve the physiological ecology of Chinese cabbage, reducing the effects of Cr stress and contributing to the global control of heavy metal pollution in food crops.

1. Introduction

Chromium (Cr) is a heavy metal element that is toxic to humans, animals, and plants. Due to its extensive use and mining activities, large amounts of Cr (VI) are released into the environment, leading to global concerns [1,2,3,4]. Prolonged exposure to Cr toxicity can adversely affect various plant processes, including seed germination, metabolism, and photosynthesis, and even lead to genotoxicity and other hazards [5,6,7,8]. Cr (VI) pollution not only disrupts plant growth and development, but also poses a risk to human health by entering the food chain [9]. Therefore, it is essential to explore new methods that can reduce Cr uptake by plants grown under Cr stress and mitigate the potential health risks associated with Cr toxicity.
The traditional methods of treating Cr in plants are often accompanied by problems such as high cost and toxicity [10]. Therefore, effective new methods are needed to improve the impact of chromium stress on plants. Se is a common mineral nutrient that is not only an essential micronutrient for animals and humans, but also promotes plant growth and increases crop yield [11]. The application of Si and Se has gradually become an innovative attempt [12]. Si is not only a beneficial element for promoting plant growth and development, but also beneficial for plant resistance to stress, which has been shown to enhance the ability of plants to cope with environmental stress [13]. The application of Si reduces the concentration of heavy metals in many plants, and related research results have shown that it can regulate the accumulation of Cr in mustard [14], reduce the accumulation of aluminum in peanuts [15], and decrease Cu toxicity in cucumber [16]. Khan et al. (2020) studied the effect of Cr stress on date palms (Phoenix dactylifera L.) mediated by Si application, suggesting that Si can effectively alleviate the Cr stress in date palm plants by reducing its accumulation and enhancing the absorption of nutrients [17]. Sarkar et al. (2020) added exogenous Si to Cr-stressed wheat, which reduced the Cr accumulation in wheat roots and significantly improved abiotic stress indicators such as total soluble protein and electrolyte leakage, fully demonstrating that Si plays an important role in the detoxification of Cr in wheat [18]. The toxicity of heavy metals, cadmium [19], and mercury [20] in leafy vegetables can be alleviated by applying low concentrations of inorganic Se in hydroponic/soil culture medium [21]. Se mitigates Cr toxicity in plants through various mechanisms, including (a) synthesizing secondary metabolites [22], (b) altering root morphology [23], (c) restoring mitochondrial function [24], and adjusting pigment content [25], among others.
In recent years, there has been an increasing number of studies investigating the application of Si and Se to crops. For instance, Huang et al. (2021) conducted an experiment in which Si and Se were added to cadmium-stressed rice, resulting in a reduction in the Cd content of the rice, demonstrating the crucial mitigation effect of Si/Se [26]. Similarly, according to Zhou et al. (2021), the application of Si and Se to wheat under Cd stress improved the antioxidant system and reduced the oxidative stress damage caused by Cd in wheat [27]. The study suggests that the addition of these exogenous elements can mitigate the negative effects of Cd stress on wheat and enhance its growth and nutritional properties. These findings have significant implications for the development of sustainable and environmentally friendly methods for managing heavy metal contamination in crops, which could have a positive impact on food security and human health.
After reviewing the current literature, we hypothesize that the exogenous application of Se and Si, either alone or in combination, to Cr-stressed Chinese cabbage could regulate the transport and distribution of Cr in plant tissues. Additionally, we propose that these treatments could enhance the antioxidant enzyme system and reduce the toxic effects of Cr on vegetables. This hypothesis is based on previous studies that have demonstrated the benefits of Se and Si in mitigating the adverse effects of heavy metals on plants, such as in the case of Cd-stressed rice and wheat. These findings suggest that Se and Si treatments could potentially have a positive impact on the growth and nutritional properties of Cr-stressed Chinese cabbage, providing a sustainable and environmentally friendly method for managing heavy metal contamination in crops.

2. Materials and Methods

2.1. Plant Culture and Experimental Design

The hydroponic experiments were conducted in a greenhouse under controlled conditions. The temperature was maintained at 25 °C, and the intensity of the white, fluorescent light was set at 225 ± 25 μmol m−2 s−1. The light/dark cycle was set to 16/8 h, and the humidity was kept between 80–85%. To begin the experiment, Chinese cabbage seeds were sterilized in a 0.5% sodium chloride solution for 30 min, rinsed with deionized water, and germinated at 25 °C for one week. Healthy and uniform seedlings were then transplanted into plastic jars (1 L) and grown in Hoagland nutrient solution. One week after transplantation, the seedlings were treated according to different treatment groups. The nutrient solution was continuously aerated and changed every three days to prevent elemental depletion [23].
A total of seven treatment groups were set up in this study and replicated three times. The concentrations of potassium dichromate, sodium metasilicate nonahydrate, and sodium selenite were set according to previous studies [28]. The specific treatments were as follows: Treatment group 1 (Cr) was treated with Hoagland nutrient solution containing 100 μmol L−1 of potassium dichromate. Treatment group 2 (Si) was treated with Hoagland’s nutrient solution containing 2.5 mmol L−1 of sodium metasilicate nonahydrate. Treatment group 3 (Se) was treated with Hoagland’s nutrient solution containing 5 μmol L−1 of sodium selenite. Treatment group 4 (Si + Cr) was treated with Hoagland nutrient solution containing 2.5 mmol L−1 of sodium metasilicate nonahydrate + 100 μmol L−1 of potassium dichromate. Treatment group 5 (Se + Cr) was treated with Hoagland nutrient solution containing 5 μmol L−1 of sodium selenite + 100 μmol L−1 of potassium dichromate. Treatment group 6 (Si + Se + Cr) was treated with Hoagland nutrient solution containing 2.5 mmol L−1 of sodium metasilicate nonahydrate + 5 μmol L−1 of sodium selenite + 100 μmol L−1 of potassium dichromate. The control group (CK) was cultured in nutrient solution. After 2 weeks of culture, the cabbage was harvested for further analysis.
After collection, the samples were soaked in a 0.5 mM CaCl2 solution for 30 min and then rinsed with deionized water. To measure the physiological and biochemical parameters, such as chlorophyll content, malondialdehyde (MDA), and glutathione (GSH), the samples were stored in an ultra-low temperature refrigerator at −80 °C. The samples were then dried at 105 °C for 0.5 h and subsequently at 80 °C until a constant weight was achieved. The dried samples were used to determine the mineral elements and Cr content.

2.2. Determination of Photosynthetic Pigments

To determine chlorophyll a (Chl a), chlorophyll b (Chl b), and carotenoid content in Chinese cabbage, the method described by Li et al. (2018) [29] was followed. Fresh Chinese cabbage (0.2 g) was ground with 5 mL of 80% (v/v) frozen acetone and placed in a TGL-20 M refrigerated centrifuge (Shanghai Luxiangyi Centrifuge Instrument Co., Ltd., Shanghai, China) at 4000 rpm for 15 min. The supernatant was then transferred to a new tube, and the residue was re-extracted with 2.5 mL of 80% (v/v) frozen acetone. Chlorophyll a, chlorophyll b, and carotenoid contents were determined using a 7600 CRT UV-Vis spectrophotometer (Shanghai Jinghua Instruments, Shanghai, China) at wavelengths of 663 nm, 645 nm, and 470 nm, respectively, and expressed in mg g−1 of fresh weight.

2.3. Oxidative Damage and Oxidative Defense Systems

The concentration of hydrogen peroxide (H2O2) was measured using the method described by Velikova et al. (2000) [30]. The Chinese cabbage samples were homogenized with 5.00 mL of 0.1% (w/v) TCA in an ice bath. The extracts were then centrifuged at 10,000 rpm for 15 min. Next, 0.50 mL of 10 mM potassium phosphate buffer (pH 7.00) and 1.00 mL of 1.00 M KI were added to 0.50 mL of the supernatant. The absorbance of the supernatant was measured at 390 nm, and the content of H2O2 was determined based on the standard curve.
MDA concentrations were determined using the method reported by Liang et al. (2008) [31]. Specifically, 2.00 mL of enzyme extract was mixed with an equal volume of 0.6% (w/v) thiobarbituric acid (TBA) and heated in a boiling water bath for 15 min. The homogenate was then cooled, snap-frozen, and centrifuged before the samples were assayed at optical densities of 450, 532, and 600 nm.
To extract the enzymatic activity from fresh shoots, 0.5 g of the shoots was ground into a fine powder in liquid nitrogen using a mortar and pestle. The powder was then transferred to another pre-cooled mortar and pestle (4 °C) containing 5 mL of 50 mmol L−1 potassium phosphate buffer (pH 7.8) that also contained 0.1 mmol L−1 of EDTA and polyvinylpolypyrrolidone. The homogenate was spun at 10,000 rpm at 4 °C for 20 min, and the enzymatic activity in the supernatant was determined using the method reported by Farooq et al. (2015) [32]. All spectrophotometric analyses were performed using a UV-Vis spectrophotometer (7600CRT, China Jinghua Instrument Company, Jinhua, China).
The POD activity was measured using a guaiacol substrate mixed with some drugs, as described by Wu et al. (2002) [33]. The assay mixture contained 1.00 mL of 0.3% H2O2, 950 μL of 0.2% guaiacol substrate, 1.00 mL of 50 mM potassium phosphate buffer (pH 7.0), and 50 μL of enzyme extract. Absorbance was recorded at 470 nm within 60 s after the addition of H2O2, and one unit of enzyme activity (U) was expressed as a 0.01 unit increase in absorbance at 470 nm within 60 s.
The CAT activity was determined by monitoring the consumption of H2O2 at 240 nm, following the method described by Cao et al. (2004) [34]. The reaction mixture contained 1.00 mL of 0.3% hydrogen peroxide, 1.95 mL of 50 mM potassium phosphate (pH 7.0), and 50 μL of enzyme extract. The CAT activity was determined based on the decrease in absorbance at 240 nm within 60 s at 25 °C, with one unit of CAT activity defined as a 0.01 unit decrease in absorbance at 240 nm.
The SOD activity was measured using the method described by Velikova et al. (2000) [30], which involves monitoring photochemical reduction inhibition using nitro blue tetrazolium (NBT). The assay mixture consisted of 2.20 mL of 50 mM potassium phosphate buffer (pH 7.80), 200 μL of 130 mM methionine, 200 μL of 75 μM NBT, 200 μL of 2 μM riboflavin, 100 μL of 0.1 mM Na2EDTA, and 100 μL of enzyme extract. The absorbance was recorded at 560 nm, and one unit of SOD activity was defined as 50% inhibition of NBT reduction.
To determine the glutathione content, the method described by Nagalakshmi et al. (2001) was followed [35]. A sample (0.2 g) was taken at a controlled temperature of 4 °C and homogenized in 2 mL of 5% TCA containing 5 mM of EDTA. The homogenate was then centrifuged at 10,000 rpm for 20 min. Approximately 100 μL of supernatant was added to 100 μL of 5% TCA and neutralized by adding 48 μL of 1.84 M triethanolamine. The absorbance was monitored at 412 nm, and the glutathione content was determined based on the standard curve. All enzymatic activity data are expressed as U g−1 fresh weight.

2.4. Nutritional Quality

The soluble protein content was determined using the method reported by Bradford (1976) [36]. Briefly, 0.2 g of the sample was taken and ground in a mortar containing 5.0 mL of phosphate buffer solution (pH 7.0). The extracts were centrifuged at 4000 rpm for 15 min, and 0.1 mL of the supernatant was mixed with 4.9 mL of Coomassie brilliant blue G-250 solution (0.1 g L−1) at 4 °C. The solubility was measured at 595 nm after 5 min, and the protein content was determined based on the standard curve.
The soluble sugar content was determined using the method reported by Fairbairn (1953) [37]. Briefly, 1.0 g of the sample was taken and mixed with 5.00 mL of distilled water. It was then placed in a water bath at 85 °C for 30 min, and the supernatant was collected. This step was repeated twice, after which 25 mL of distilled water was added. Next, 1.00 mL of the extract was mixed with 5.00 mL of anthrone sulfate solution and completely mixed. The mixture was kept at 85 °C for 5 min, and the optical density was measured at 620 nm. A glucose standard curve was prepared, and the soluble sugar content was determined based on the standard curve.

2.5. Determination of Mineral Element Content and Cr Content

The content of mineral elements in plants was determined according to the method reported by Gao et al. (2022) [38]. First, 0.2 g of the dry sample was accurately weighed into a 25 mL conical flask, and 1 mL of deionized water was added to wet the sample. Then, 5 mL of concentrated sulfuric acid was added, and the mixture was digested on an electric hotplate (200 °C) after 24 h. When white smoke started to appear, H2O2 was added until the digestive fumes were clear. After cooling, the digested solution was rinsed into a 50 mL volumetric flask, filtered through a 0.22 µm water membrane, and the N and P contents measured using a discrete autoanalyzer (Smart chem 200, Alliance, France). Next, 0.2 g of the dry sample was accurately weighed into a digestion tube, and 10 mL of HNO3:HClO4 (4:1 v/v) was added. The mixture was digested using a microwave accelerated reaction system MARS6 (CEM, Matthews, Charlotte, NC, USA), cooled, and rinsed to the volume of a 50 mL bottle. It was then filtered through a 0.22 µm water membrane and determined for K, Ca, and Mg.
The Cr concentrations in plants were determined according to the method reported by Qing et al. (2015) [39]. After the wet digestion of the samples in an HNO3:HClO4 mixture, the Cr concentration was determined using flame atomic absorption spectrometry (AA6300, Shimadzu, Kyoto, Japan).

2.6. Proline Determination

To determine the proline content, the method reported by Qing et al. (2015) was followed [39]. Approximately 0.5 g of leaves was extracted with 5 mL of aqueous sulfosalicylic acid (3%) and filtered. Then, 2 mL of the reaction mixture was reacted with 2 mL of glacial acetic acid and 2 mL of ninhydrin. The reaction mixture was heated in a boiling water bath for 30 min and cooled to room temperature. After that, 4 mL of toluene was added and mixed vigorously. The toluene layer was then separated, and the absorbance was measured spectrophotometrically at 520 nm. The proline content was determined from a standard curve prepared by optical densitometric determination of the proline concentration, and the results were expressed as μg g−1 FW plant tissue.

2.7. Data Analysis

The experimental data were analyzed using SPSS 25.0 (SPSS Inc., Chicago, IL, USA), and the values were expressed as the mean ± SE of three replicates. A principal component analysis (PCA) was performed using the R version 4.2.2 (31 October 2022) with the factoextra package for data visualization. All data matrices were auto-scaled before the analysis. The differences between the treatment groups were analyzed by LSD multiple comparisons, with a probability of p < 0.05.

3. Results

3.1. Effects of Si and Se on Cr Content in Chinese Cabbage under Chromium Stress

With the induction of phytotoxicity by Cr, the Cr content in Chinese cabbage increased significantly (Figure 1). Chromium was not detected in the control group, and the chromium content in plants under chromium stress was 68.05 mg kg−1. The Cr contents were significantly reduced with the addition of Si + Se treatment (73.99%) compared with the Cr-only treatments. Moreover, the Si and Se treatments were also found to significantly reduce the Cr content compared with the Cr-only treatment.

3.2. Effects of Si and Se on the Photosynthetic Pigments in Cabbage Treated with Cr

Si and Se increased the chlorophyll content in Chinese cabbage under Cr stress (Figure 2A–C). The single chromium treatment significantly reduced the content of chlorophyll a, chlorophyll b, and carotenoids in cabbage leaves by 18.84%, 26.17%, and 21.15%, respectively. The content of chlorophyll a increased by 25.07%, 51.79%, and 62.50%, respectively; the content of chlorophyll b increased by 23.98%, 28.51%, and 47.51%, respectively; and the content of carotenoids increased by 13.24%, 17.07%, and 27.00%, respectively, with the addition of Si, Se, Si + Se to Chinese cabbage under chromium stress.

3.3. Mitigation of Si and Se on Redox of Chinese Cabbage under Cr Stress (MDA, H2O2)

Compared with the control group, Cr-treated MDA and H2O2 activities significantly increased by 60.66% and 18.57%, respectively (Figure 3A,B). However, the Si or Se treatment reduced these oxidative stress parameters in Cr-treated plants. Compared with Cr treatment, the combined application of Si and Se had the greatest decrease in these traits, with MDA and H2O2 activities being 24.15% and 23.41%, respectively.

3.4. Effects of Si and Se on Antioxidant Enzyme Activity (SOD, CAT, POD) of Chinese Cabbage under Chromium Stress

Cr, Se, and Si all affected the activity of antioxidant enzymes, including SOD, CAT, and POD. Compared with the control condition, due to exogenous chromium stress, the activities of different antioxidant enzymes in Chinese cabbage were enhanced, and the activities of SOD, CAT, and POD were increased (15.57, 18.30, 31.50%) (Figure 4A–C). The supply of Si or Se led to an increase in the SOD, CAT, and POD content of the Cr treatment. The maximum increase in SOD was 28.21%, the maximum increase in CAT was 7.55%, and the maximum increase in POD was 21.37% in Chinese cabbage treated with Si and Se stress.

3.5. Effects of Si and Se Application on Non-Enzymatic Antioxidants in Chinese Cabbage under Chromium Stress (Proline, GSH)

In Chinese cabbage, exogenous chromium significantly increased the content of proline by 52.67% and only increased the content of GSH by 1.51% compared with the control group (Figure 5A,B). The supply of Si or Se resulted in a decrease in the Cr-treated proline content and an increase in the GSH content. A 27.44% decrease in proline and a 28.51% increase in GSH were observed in the chromium-stressed cabbage treated with Si and Se alone, compared to the chromium-only treated cabbage.

3.6. Effects of Silicon and Selenium on the Nutritional Quality of Chromium-Treated Cabbage (Protein, Sugar)

Compared with the untreated control group, the Cr treatment significantly reduced the contents of soluble protein (17.44%) and soluble sugar (67.32%) in Chinese cabbage (Figure 6A,B). Applying Si and Se (Si + Cr and Se + Cr) alone in plants subjected to chromium stress can effectively alleviate the effects of Cr stress on Chinese cabbage, increasing water-soluble protein (13.38 and 16.90%) and soluble sugar (40.6 and 60.93%). Under Cr stress conditions, the Si + Se + Cr combination treatment, respectively, increased the soluble protein (29.58%) and soluble sugar (134.37%) in Chinese cabbage, and more obviously alleviated Cr stress (Figure 6A,B). These results indicate that under Cr stress, the Si + Se combined treatment can more significantly improve Cr-induced redox stress than Si or Se alone.

3.7. Effects of Silicon and Selenium on the Content of Mineral Elements in Chromium-Treated Cabbage (N/P/K/Ca/Mg)

Compared with the control group without any treatment, the chromium treatment reduced the accumulation of mineral elements, namely N, P, K, Ca, and Mg (by 17.25, 27.36, 27.03, 2.73, and 9.31%) (Figure S1A–E). In this study, the presence of Si or Se could increase the mineral element content of cabbage. Exogenous Si or Se can promote the accumulation of N, P, K, Ca, Mg, and other mineral elements in Chinese cabbage under chromium stress. Compared with the plants treated with chromium alone, Si + Se repaired plant minerals caused by chromium stress by increasing N, P, K, Ca, and Mg (by about 31.72, 37.68, 28.87, 16.82, and 24.90%) in cabbage.

3.8. Principal Component Analysis

Figure 7 illustrates the treatments and variables plot in the principal component analysis (PCA) projection of PC1 and PC2, which took into account all the properties measured and the calculated parameters. PC1 accounted for 60.1% of the variance, while PC2 accounted for 24.8% of the variance. The figure revealed high positive correlations between chlorophyll contents, macro and micronutrients, GSH, and sugar. Moreover, the properties of the Si and Cr treatments were mainly shaped by P, K, and sugar. The results of the study demonstrated that the application of the Si and Se treatments to Cr-contaminated plants led to a significant improvement in their physiological and nutritional values. The improvement was likely due to lower oxidative stress in plants and the provision of nutrients that are required for photosynthesis [40]. Heavy metal stress causes oxidative stress and impairment in plant nutrients, which affects their physiological and nutritional values [41]. Therefore, the results suggest that the application of Si and Se treatments can mitigate the negative effects of heavy metal stress on plant growth and nutrition. Overall, this study highlights the potential benefits of Si and Se treatments in improving the physiological and nutritional values of Cr-contaminated plants. The findings of the study have implications for the development of sustainable and environmentally friendly methods for managing heavy metal contamination in plants, which could have significant implications for food security and human health.

4. Discussion

The chromium content in plants can directly reflect the degree of chromium stress on plants by heavy metals. In general, a lower heavy metal content indicates lower toxicity and better crop growth [42]. In this study, silicon, selenium, and the silicon–selenium compound treatment reduced the chromium content in cabbage. The synergistic effect of silicon and selenium showed that the chromium content in cabbage was even lower than that of silicon or selenium alone (Figure 1), which may be the most direct reason for the stronger photosynthesis after adding silicon and selenium (Figure 2A–C). Silicon, selenium, and the silicon–selenium compound treatment may reduce the toxic accumulation of chromium by affecting the accumulation and transport of chromium. The research results of Zeng et al. (2011) showed that exogenous silicon reduces the toxicity of chromium in rice, mainly by forming a complex with chromium or depositing chromium on the cell wall [28]. Qing et al. (2015) believed that exogenous selenium changed the distribution of chromium in leaf subcells, thereby chelating and separating metal ions and slowing the toxic effect of chromium on cell activity [39]. The research results of Huang et al. (2021) showed that the synergistic effect of silicon and selenium can promote the binding of cadmium in the cell wall and the transportation of chelated cadmium to the vacuole, thereby reducing the toxicity of cadmium, which is consistent with the results of this study [26].
The reduction in light-harvesting components (chlorophyll a, chlorophyll b, carotenoids) is one of the important reasons for the reduction in plant biomass under chromium stress. For example, the research results of Chauhan et al. (2017) showed that when adding exogenous Se to chromium-treated plants, the accumulation of plant biomass is enhanced by increasing the synthesis of chlorophyll pigments [43]. Related research results show that the activity of chlorophyll-producing enzymes may be reduced under the condition of chromium stress in plants, which damages the pathway of plant synthesis of chlorophyll pigments and leads to light capture in plants. Moreover, the pigment (chlorophyll a, chlorophyll b, and carotenoid) content decreased [12]. The application of silicon and selenium increased the chlorophyll and carotenoid content in plants that were exposed to chromium stress. This suggests that the treatment with exogenous selenium, silicon, and the silicon-selenium compound is beneficial for protecting chlorophyll in plants. This protective effect is achieved by improving the accumulation of chromium, respiration rate, and biosynthesis of light-harvesting pigments. The increase in chlorophyll and carotenoid content is an indication that the plants are better able to withstand the oxidative stress caused by chromium toxicity. The results of Manzoor et al. (2022) showed that nano-silicon can improve the photosynthetic efficiency of wheat plants under external chromium stress; the biomass increased at the same time as the chlorophyll content, which is consistent with our results [44]. In addition, according to the report of Handa et al. (2018b), exogenous selenium can effectively slow the degradation of chlorophyll in mustard greens [25]. According to the results of Saidi et al. (2014), the addition of source selenium increases carotenoids (a scavenger of singlet oxygen species) in plants, thereby inhibiting the generation of reactive oxygen species in sunflower under cadmium stress [45]. Compared with the single treatment group of silicon and selenium, the combined treatment of the silicon and selenium group significantly increased the content of chlorophyll and carotenoids. The results of Huang et al. (2021) showed that the combined treatment of silicon and selenium significantly restored the content of photosynthetic pigments in plants subjected to cadmium stress, which is consistent with the results of this study [26].
According to Gill et al. (2015), the exposure of cabbage to chromium stress resulted in a significant increase in the levels of active oxygen species H2O2 and MDA (Figure 3A,B), which can cause damage to plant tissue cells. This was attributed to the adverse effects of chromium stress on the cabbage plants [46]. Singh et al. (2013) also reported that heavy metals can interact with electron transport chain carriers, leading to the accumulation of ROS in plants, which in turn promotes lipid peroxidation and damages the integrity of plant cell membranes [47].
In contrast, treatment with a combination of silicon, selenium, and silicon–selenium compounds was found to decrease the levels of MDA and H2O2 in cabbage compared to the group treated with chromium alone (Figure 3A,B). This can be attributed to the ability of these exogenous compounds to mitigate oxidative damage induced by chromium stress by reducing the production of ROS and protecting the integrity of the cell membrane by inhibiting lipid peroxidation. The results of Manzoor et al. (2022) showed that the effective reduction in nano-silica could reduce the content of MDA and H2O2 in Cr-stressed rice plants [41]. According to the research results of Handa et al. (2019), adding a certain amount of exogenous selenium to mustard under chromium stress can alleviate the damage to the mustard membrane, as well as minimize the content of MDA and H2O2 in the plant, which also promotes the further absorption of nutrients by the plant [22]. The research results of Huang et al. (2021) showed that the combined treatment of exogenous silicon and selenium can effectively reduce the MDA content in plants under cadmium stress, which is consistent with the results of this study [26].
Plant cells can reduce the active oxygen produced in the body when the plant is under external stress by enhancing its own antioxidant defense system. The research results showed that the activities of POD, SOD, and CAT in plants were significantly increased under chromium stress (Figure 4A–C), which is the change of the antioxidant defense system in response to external chromium stress. Under the condition of chromium stress, exogenous silicon, selenium, and the silicon–selenium compound treatment increased the activity of antioxidant enzymes SOD, POD, and CAT in cabbage (Figure 4A–C). The increase in antioxidant enzyme activity indicated that exogenous silicon, selenium, and the silicon–selenium compound treatment could improve plant tolerance to chromium and maintain the plant’s own redox balance by inhibiting the excessive production of ROS produced by plants under chromium stress. Relevant research results show that adding exogenous selenium to plants stressed by heavy metals such as cadmium and lead can effectively enhance the activity of antioxidant enzymes in plants [48]. The research results of Tripathi et al. (2015) showed that the content of SOD, POD, and CAT in plants increased after adding exogenous nano-silicon to plants under chromium stress, thereby alleviating the adverse effects of chromium stress on lipid peroxidation and H2O2 accumulation in plants [49]. The results of Riaz et al. (2021) showed that the combined application of silicon and selenium significantly alleviated the oxidative damage of heavy metals to plants by maintaining an effective defense system [50].
Proline is a common osmotic pressure-regulating substance in plants. It maintains redox metabolism by removing excess reactive oxygen species in plants. Proline synthesis promotes the plant redox cycle and helps to maintain the antioxidant defense mechanism of plants under external stress. Under the condition of chromium stress, selenium, silicon, and the silicon–selenium compound treatment weakened chromium stress and decreased proline synthesis (Figure 5A). These results confirm that silicon, selenium, and the silicon–selenium compound treatment can control ROS by initiating other antioxidant defense mechanisms, and plants do not need excessive proline to eliminate ROS produced by plants under heavy metal stress. The research results of Shinde et al. (2016) showed that in rice plants subjected to chromium stress, the proline content decreased after the addition of exogenous silicon, which is consistent with the conclusion of this study [51]. The research results of Qing et al. (2015) showed that the application of selenium did not change the effect of chromium on the content of proline or the accumulation product of osmoregulation; on the contrary, the addition of exogenous selenium reduced the content of proline in plants under chromium stress [39]. Nahar et al. (2015) believed that non-enzyme antioxidant GSH contains sulfhydryl (−SH), which plays an important role in the detoxification process of heavy metals [52]. Under excessive chromium stress, the GSH content in Chinese cabbage increased significantly to alleviate the effects of chromium stress. In this study, silicon, selenium, and the silicon–selenium compound treatment increased the glutathione content in Chinese cabbage (Figure 5B). The results of Rahman et al. (2017) showed that the addition of silicon can effectively increase the GSH content in pea under cadmium stress [53]. The results of Kumar et al. (2012) showed that the addition of exogenous selenium can promote the synthesis of GSH in plants and effectively increase the GSH content in red seaweed Gracilaria under cadmium stress [54]. The research results of Huang et al. (2021) showed that the combined use of silicon and selenium increases the GSH content in rice under cadmium stress, which is consistent with the conclusion of this study [26].
Compared with the blank control group, the protein/soluble protein content of cabbage was significantly reduced under chromium stress, which may be due to the oxidative damage of plants caused by chromium stress, resulting in a significant decrease in soluble protein/soluble protein content in plants. However, exogenous silicon, selenium, and the silicon–selenium compound treatments alleviated this stress by reducing the uptake and accumulation of chromium (Figure 6A,B). The results of Ashfaque et al. (2017) showed that silicon has a positive effect on stabilizing protein content under various abiotic stresses and effectively alleviate the decline in soluble protein content caused by chromium stress [14]. The research results of Ulhassan et al. (2019) showed that plant amino acids decreased under chromium stress, which led to the decrease in protein in plants, and exogenous selenium promoted the amino acid levels in Brassica napus tissues under chromium stress, thereby increasing the protein content in plants [12]. Soluble sugars serve as important metabolic substrates with dynamic roles in many processes controlling plant developmental stages [55]. It is known that under environmental stress conditions, the level of soluble sugar in plants is controlled by the rate of photosynthesis, and exogenous chromium leads to a decrease in the content of soluble sugar in plants [56]. Relevant research results show that the reduction in soluble sugar content in plants under heavy metal stress is due to the destruction of chloroplasts and the subsequent reduction in photosynthetic activity [57]. When plants are under chromium stress, the exogenous application of silicon, selenium, and the silicon–selenium compound treatment can increase photosynthetic efficiency by maintaining a higher level of sugar, which may help to alleviate the effects of Cr stress on plants by promoting the production of energy and metabolites damage. The research conclusion of Yang et al. (2021) showed that rice seedlings subjected to chromium stress were supplemented with exogenous silicon, and the soluble sugar content increased compared with the chromium single treatment group [58]. The research results of Sardar et al. (2022) showed that nano-selenium can alleviate the cadmium stress and maintain the physiological and chemical activities of plants by consuming a certain amount of soluble sugar [57].
At present, there are relatively few studies on the absorption of plant nutrients by the addition of exogenous selenium and silicon. As predicted before the experiment, under the single chromium treatment, the content of trace elements and macroelements in plants decreased significantly. The research results of Handa et al. (2018a) showed that excess chromium may replace the absorption and transport of nutrients, which is mainly due to the ionic similarity between chromium and essential elements (N, P, K, Ca, Mg), etc., whose content decreased further [59]. However, silicon and selenium showed the ability to increase the content of mineral nutrients under chromium stress, and the content of nutrients in plants in the silicon and selenium compound treatment group increased significantly compared with the single chromium treatment group (Figure S1A–E). This may be because the exogenous addition of silicon, selenium, and the silicon–selenium compound treatment to plants effectively reduces lipid peroxidation, and H2O2 production slows the damage of cabbage cell membranes caused by chromium stress, thereby enhancing the absorption capacity of mineral nutrients in plants under chromium stress [10]. The results of Ulhassan et al. (2022) showed that nano-silicon reduced the inhibitory effect of chromium stress on the absorption of plant nutrients [60]. The research results of Handa et al. (2018a) showed that after supplementing selenium to mustard under chromium stress, exogenous selenium can improve the content of mineral nutrients in mustard, reduce the absorption of chromium by mustard seedlings, and enhance the tolerance to chromium stress [56]. The research results of Riaz et al. (2021) showed that cadmium poisoning led to a decrease in nutrient content, while the application of selenium and silicon relieved the symptoms of cadmium toxicity in leaves and roots and increased the content of plant mineral nutrients [47]. The results of this study show that the single or combined treatment of silicon and selenium can improve the absorption of chromium stress on the nutrient elements of Chinese cabbage, and the combined treatment has the best effect, which is consistent with the previous research results.

5. Conclusions

The addition of silicon and selenium had a synergistic effect in alleviating the harmful effects of chromium stress on cabbage. The simultaneous use of Si and Se has been found to enhance cabbage growth and productivity by increasing the content of photosynthetic pigments, promoting photosynthesis, improving the uptake of essential minerals and nutrients, and boosting the plant’s ability to withstand unfavorable environmental conditions. Additionally, it reduces oxidative stress in cabbage by lowering the oxide content, increasing antioxidant enzyme activity, and reducing non-enzymatic antioxidants. Restoring cabbage under chromium stress will also provide valuable scientific support for controlling heavy metal pollution and ensuring food crop safety globally.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/su15065361/s1, Figure S1: Effects of exogenous selenium (Se) (5 μmol L−1) and silicon (Si) (2.5 mmol L−1), individually or in combination, on the contents of N (g/100 g) (A), P (mg kg−1) (B), K (mg kg−1) (C), and Ca (mg kg−1) (D), Mg (mg kg−1) (E) in the chromium (Cr) (0, 100 μmol L−1) treated Chinese cabbage. Bars indicate the standard deviation (SD) of the mean (n = 3), and different lowercase letters indicate significant differences among treatments (p < 0.05).

Author Contributions

Conceptualization, X.F. (Xiuxian Fu) and S.M.; methodology, X.F. (Xiuxian Fu); software, X.F. (Xiuxian Fu); validation, W.A., S.M. and W.O.; formal analysis, X.F. (Xiuxian Fu); investigation, X.F. (Xiuhao Fu); resources, P.S.; data curation, X.F. (Xiuxian Fu); writing—original draft preparation, X.F. (Xiuxian Fu), S.M. and Q.Z.; writing—review and editing, X.F. (Xiuxian Fu), S.M. and X.F. (Xiuxian Fu); visualization, Z.S.; supervision, Z.S. and W.L. All authors have read and agreed to the published version of the manuscript.

Funding

This study was partially supported by The National Natural Science Foundation of China (NSFC-31860728), the specific research fund of The Innovation Platform for Academicians of Hainan Province (YSPTZX20212), Key R & D projects in Hainan Province (ZDYF2021XDNY185), and the Hainan Province Science and Technology Special Fund (ZDYF2021SHFZ071).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

This paper and its Supplementary Information contain all relevant data.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Ao, M.; Chen, X.; Deng, T.; Sun, S.; Tang, Y.; Morel, J.L.; Qiu, R.; Wang, S. Chromium Biogeochemical Behaviour in Soil-Plant Systems and Remediation Strategies: A Critical Review. J. Hazard. Mater. 2021, 424, 127233. [Google Scholar] [CrossRef] [PubMed]
  2. Mehmood, S.; Mahmood, M.; Núñez-Delgado, A.; Alatalo, J.M.; Elrys, A.S.; Rizwan, M.; Weng, J.; Li, W.; Ahmed, W. A Green Method for Removing Chromium (VI) from Aqueous Systems Using Novel Silicon Nanoparticles: Adsorption and Interaction Mechanisms. Environ. Res. 2022, 213, 113614. [Google Scholar] [CrossRef] [PubMed]
  3. Mehmood, S.; Ahmed, W.; Rizwan, M.; Imtiaz, M.; Mohamed Ali Elnahal, A.S.; Ditta, A.; Irshad, S.; Ikram, M.; Li, W. Comparative Efficacy of Raw and HNO3-Modified Biochar Derived from Rice Straw on Vanadium Transformation and Its Uptake by Rice (Oryza sativa L.): Insights from Photosynthesis, Antioxidative Response, and Gene-Expression Profile. Environ. Pollut. 2021, 289, 117916. [Google Scholar] [CrossRef] [PubMed]
  4. Mehmood, S.; Ahmed, W.; Ikram, M.; Imtiaz, M.; Mahmood, S.; Tu, S.; Chen, D. Chitosan Modified Biochar Increases Soybean (Glycine max L.) Resistance to Salt-Stress by Augmenting Root Morphology, Antioxidant Defense Mechanisms and the Expression of Stress-Responsive Genes. Plants 2020, 9, 1173. [Google Scholar] [CrossRef] [PubMed]
  5. Kapoor, R.T.; Bani Mfarrej, M.F.; Alam, P.; Rinklebe, J.; Ahmad, P. Accumulation of Chromium in Plants and Its Repercussion in Animals and Humans. Environ. Pollut. 2022, 301, 119044. [Google Scholar] [CrossRef]
  6. Srivastava, D.; Tiwari, M.; Dutta, P.; Singh, P.; Chawda, K.; Kumari, M.; Chakrabarty, D. Chromium Stress in Plants: Toxicity, Tolerance and Phytoremediation. Sustainability 2021, 13, 4629. [Google Scholar] [CrossRef]
  7. Shanker, A.K.; Cervantes, C.; Loza-Tavera, H.; Avudainayagam, S. Chromium Toxicity in Plants. Environ. Int. 2005, 31, 739–753. [Google Scholar] [CrossRef]
  8. Martinelli, F.; Colzi, I.; Gonnelli, C.; Vergata, C.; Golia, G.; Coppi, A.; Castellani, M.B.; Giovino, A.; Buti, M.; Sabato, T.; et al. Transgenerational Effects of Chromium Stress at Phenotypic and Molecular Level in Arabidopsis Thaliana. J. Hazard. Mater. 2023, 442, 130092. [Google Scholar] [CrossRef]
  9. Pushkar, B.; Sevak, P.; Parab, S.; Nilkanth, N. Chromium Pollution and Its Bioremediation Mechanisms in Bacteria: A Review. J. Environ. Manag. 2021, 287, 112279. [Google Scholar] [CrossRef]
  10. Fernández, P.M.; Viñarta, S.C.; Bernal, A.R.; Cruz, E.L.; Figueroa, L.I.C. Bioremediation Strategies for Chromium Removal: Current Research, Scale-up Approach and Future Perspectives. Chemosphere 2018, 208, 139–148. [Google Scholar] [CrossRef]
  11. Zhu, Y.; Dong, Y.; Zhu, N.; Jin, H. Foliar Application of Biosynthetic Nano-Selenium Alleviates the Toxicity of Cd, Pb, and Hg in Brassica Chinensis by Inhibiting Heavy Metal Adsorption and Improving Antioxidant System in Plant. Ecotoxicol. Environ. Saf. 2022, 240, 113681. [Google Scholar] [CrossRef]
  12. Ulhassan, Z.; Gill, R.A.; Huang, H.; Ali, S.; Mwamba, T.M.; Ali, B.; Huang, Q.; Hamid, Y.; Khan, A.R.; Wang, J.; et al. Selenium Mitigates the Chromium Toxicity in Brassicca napus L. by Ameliorating Nutrients Uptake, Amino Acids Metabolism and Antioxidant Defense System. Plant Physiol. Biochem. 2019, 145, 142–152. [Google Scholar] [CrossRef]
  13. Chen, D.; Chen, D.; Xue, R.; Long, J.; Lin, X.; Lin, Y.; Jia, L.; Zeng, R.; Song, Y. Effects of Boron, Silicon and Their Interactions on Cadmium Accumulation and Toxicity in Rice Plants. J. Hazard. Mater. 2018, 367, 447–455. [Google Scholar] [CrossRef]
  14. Ashfaque, F.; Inam, A.; Inam, A.; Iqbal, S.; Sahay, S. Response of Silicon on Metal Accumulation, Photosynthetic Inhibition and Oxidative Stress in Chromium-Induced Mustard (Brassica juncea L.). S. Afr. J. Bot. 2017, 111, 153–160. [Google Scholar] [CrossRef]
  15. Zhao, K.; Yang, Y.; Zhang, L.; Zhang, J.; Zhou, Y.; Huang, H.; Luo, S.; Luo, L. Silicon-Based Additive on Heavy Metal Remediation in Soils: Toxicological Effects, Remediation Techniques, and Perspectives. Environ. Res. 2022, 205, 112244. [Google Scholar] [CrossRef] [PubMed]
  16. Bosnić, D.; Nikolić, D.; Timotijević, G.; Pavlović, J.; Vaculík, M.; Samardžić, J.; Nikolić, M. Silicon Alleviates Copper (Cu) Toxicity in Cucumber by Increased Cu-Binding Capacity. Plant Soil 2019, 441, 629–641. [Google Scholar] [CrossRef]
  17. Khan, A.; Bilal, S.; Khan, A.L.; Imran, M.; Al-Harrasi, A.; Al-Rawahi, A.; Lee, I.J. Silicon-Mediated Alleviation of Combined Salinity and Cadmium Stress in Date Palm (Phoenix dactylifera L.) by Regulating Physio-Hormonal Alteration. Ecotoxicol. Environ. Saf. 2020, 188, 109885. [Google Scholar] [CrossRef]
  18. Sarkar, U.; Tahura, S.; Das, U.; Amin Mintu, M.R.; Kabir, A.H. Mitigation of Chromium Toxicity in Wheat (Triticum aestivum L.) Through Silicon. Gesunde Pflanz. 2020, 72, 237–244. [Google Scholar] [CrossRef]
  19. Yu, Y.; Yuan, S.; Zhuang, J.; Wan, Y.; Wang, Q.; Zhang, J.; Li, H. Effect of Selenium on the Uptake Kinetics and Accumulation of and Oxidative Stress Induced by Cadmium in Brassica Chinensis. Ecotoxicol. Environ. Saf. 2018, 162, 571–580. [Google Scholar] [CrossRef] [PubMed]
  20. Tran, T.A.T.; Dinh, Q.T.; Cui, Z.; Huang, J.; Wang, D.; Wei, T.; Liang, D.; Sun, X.; Ning, P. Comparing the Influence of Selenite (Se4+) and Selenate (Se6+) on the Inhibition of the Mercury (Hg) Phytotoxicity to Pak Choi. Ecotoxicol. Environ. Saf. 2018, 147, 897–904. [Google Scholar] [CrossRef] [PubMed]
  21. Shekari, L.; Aroiee, H.; Mirshekari, A.; Nemati, H. Protective Role of Selenium on Cucumber (Cucumis sativus L.) Exposed to Cadmium and Lead Stress during Reproductive Stage Role of Selenium on Heavy Metals Stress. J. Plant Nutr. 2019, 42, 529–542. [Google Scholar] [CrossRef]
  22. Handa, N.; Kohli, S.K.; Sharma, A.; Thukral, A.K.; Bhardwaj, R.; Abd_Allah, E.F.; Alqarawi, A.A.; Ahmad, P. Selenium Modulates Dynamics of Antioxidative Defence Expression, Photosynthetic Attributes and Secondary Metabolites to Mitigate Chromium Toxicity in Brassica juncea L. Plants. Environ. Exp. Bot. 2018, 161, 180–192. [Google Scholar] [CrossRef]
  23. Zhao, Y.; Hu, C.; Wang, X.; Qing, X.; Wang, P.; Zhang, Y.; Zhang, X.; Zhao, X. Selenium Alleviated Chromium Stress in Chinese Cabbage (Brassica campestris L. Ssp. Pekinensis) by Regulating Root Morphology and Metal Element Uptake. Ecotoxicol. Environ. Saf. 2019, 173, 314–321. [Google Scholar] [CrossRef]
  24. Nie, M.; Hu, C.; Shi, G.; Cai, M.; Wang, X.; Zhao, X. Selenium Restores Mitochondrial Dysfunction to Reduce Cr-Induced Cell Apoptosis in Chinese Cabbage (Brassica campestris L. Ssp. Pekinensis) Root Tips. Ecotoxicol. Environ. Saf. 2021, 223, 112564. [Google Scholar] [CrossRef] [PubMed]
  25. Handa, N.; Kohli, S.K.; Sharma, A.; Thukral, A.K.; Bhardwaj, R.; Alyemeni, M.N.; Wijaya, L.; Ahmad, P. Selenium Ameliorates Chromium Toxicity through Modifications in Pigment System, Antioxidative Capacity, Osmotic System, and Metal Chelators in Brassica Juncea Seedlings. S. Afr. J. Bot. 2018, 119, 1–10. [Google Scholar] [CrossRef]
  26. Huang, H.; Li, M.; Rizwan, M.; Dai, Z.; Yuan, Y.; Hossain, M.M.; Cao, M.; Xiong, S.; Tu, S. Synergistic Effect of Silicon and Selenium on the Alleviation of Cadmium Toxicity in Rice Plants. J. Hazard. Mater. 2020, 401, 123393. [Google Scholar] [CrossRef] [PubMed]
  27. Zhou, J.; Zhang, C.; Du, B.; Cui, H.; Fan, X.; Zhou, D.; Zhou, J. Soil and Foliar Applications of Silicon and Selenium Effects on Cadmium Accumulation and Plant Growth by Modulation of Antioxidant System and Cd Translocation: Comparison of Soft vs. Durum Wheat Varieties. J. Hazard. Mater. 2021, 402, 123546. [Google Scholar] [CrossRef]
  28. Zeng, F.R.; Zhao, F.S.; Qiu, B.Y.; Ouyang, Y.N.; Wu, F.B.; Zhang, G.P. Alleviation of Chromium Toxicity by Silicon Addition in Rice Plants. Agric. Sci. China 2011, 10, 1188–1196. [Google Scholar] [CrossRef]
  29. Li, X.; Ke, M.; Zhang, M.; Peijnenburg, W.J.G.M.; Fan, X.; Xu, J.; Zhang, Z.; Lu, T.; Fu, Z.; Qian, H. The Interactive Effects of Diclofop-Methyl and Silver Nanoparticles on Arabidopsis Thaliana: Growth, Photosynthesis and Antioxidant System. Environ. Pollut. 2018, 232, 212–219. [Google Scholar] [CrossRef]
  30. Velikova, V.; Yordanov, I.; Edreva, A. Oxidative Stress and Some Antioxidant Systems in Acid Rain-Treated Bean Plants Protective Role of Exogenous Polyamines. Plant Sci. 2000, 151, 59–66. [Google Scholar] [CrossRef]
  31. Liang, Y.; Zhu, J.; Li, Z.; Chu, G.; Ding, Y.; Zhang, J.; Sun, W. Role of Silicon in Enhancing Resistance to Freezing Stress in Two Contrasting Winter Wheat Cultivars. Environ. Exp. Bot. 2008, 64, 286–294. [Google Scholar] [CrossRef]
  32. Farooq, M.A.; Li, L.; Ali, B.; Gill, R.A.; Wang, J.; Ali, S.; Gill, M.B.; Zhou, W. Oxidative Injury and Antioxidant Enzymes Regulation in Arsenic-Exposed Seedlings of Four Brassica napus L. Cultivars. Environ. Sci. Pollut. Res. 2015, 22, 10699–10712. [Google Scholar] [CrossRef] [PubMed]
  33. Wu, Y.X.; von Tiedemann, A. Impact of Fungicides on Active Oxygen Species and Antioxidant Enzymes in Spring Barley (Hordeum vulgare L.) Exposed to Ozone. Environ. Pollut. 2002, 116, 37–47. [Google Scholar] [CrossRef] [PubMed]
  34. Cao, X.; Ma, L.Q.; Tu, C. Antioxidative Responses to Arsenic in the Arsenic-Hyperaccumulator Chinese Brake Fern (Pteris vittata L.). Environ. Pollut. 2004, 128, 317–325. [Google Scholar] [CrossRef]
  35. Nagalakshmi, N.; Prasad, M.N.V. Responses of Glutathione Cycle Enzymes and Glutathione Metabolism to Copper Stress in Scenedesmus Bijugatus. Plant Sci. 2001, 160, 291–299. [Google Scholar] [CrossRef]
  36. Bradford, M. A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Anal. Biochem. 1976, 72, 248–254. [Google Scholar] [CrossRef]
  37. Brooks, J.R.; Griffin, V.K.; Kattan, M.W. A Modified Method for Total Carbohydrate Analysis of Glucose Syrups, Maltodextrins, and Other Starch Hydrolysis Products. Cereal Chem. 1986, 63, 465–466. [Google Scholar]
  38. Gao, S.; Kong, Y.; Lv, Y.; Cao, B.; Chen, Z.; Xu, K. Effect of Different LED Light Quality Combination on the Content of Vitamin C, Soluble Sugar, Organic Acids, Amino Acids, Antioxidant Capacity and Mineral Elements in Green Onion (Allium fistulosum L.). Food Res. Int. 2022, 156, 111329. [Google Scholar] [CrossRef]
  39. Qing, X.; Zhao, X.; Hu, C.; Wang, P.; Zhang, Y.; Zhang, X.; Wang, P.; Shi, H.; Jia, F.; Qu, C. Selenium Alleviates Chromium Toxicity by Preventing Oxidative Stress in Cabbage (Brassica campestris L. Ssp. Pekinensis) Leaves. Ecotoxicol. Environ. Saf. 2015, 114, 179–189. [Google Scholar] [CrossRef]
  40. Hussain, A.; Rizwan, M.; Ali, Q.; Ali, S. Seed Priming with Silicon Nanoparticles Improved the Biomass and Yield While Reduced the Oxidative Stress and Cadmium Concentration in Wheat Grains. Environ. Sci. Pollut. Res. 2019, 26, 7579–7588. [Google Scholar] [CrossRef]
  41. Shi, Z.; Yang, S.; Han, D.; Zhou, Z.; Li, X.; Liu, Y.; Zhang, B. Silicon Alleviates Cadmium Toxicity in Wheat Seedlings (Triticum aestivum L.) by Reducing Cadmium Ion Uptake and Enhancing Antioxidative Capacity. Environ. Sci. Pollut. Res. 2018, 25, 7638–7646. [Google Scholar] [CrossRef] [PubMed]
  42. Wu, Z.; Wang, F.; Liu, S.; Du, Y.; Li, F.; Du, R.; Wen, D.; Zhao, J. Comparative Responses to Silicon and Selenium in Relation to Cadmium Uptake, Compartmentation in Roots, and Xylem Transport in Flowering Chinese Cabbage (Brassica campestris L. Ssp. Chinensis Var. Utilis) under Cadmium Stress. Environ. Exp. Bot. 2016, 131, 173–180. [Google Scholar] [CrossRef]
  43. Chauhan, R.; Awasthi, S.; Tripathi, P.; Mishra, S.; Dwivedi, S.; Niranjan, A.; Mallick, S.; Tripathi, P.; Tripathi, R.D.; Chauhan, R.; et al. Selenite Modulates the Level of Phenolics and Nutrient Element to Alleviate the Toxicity of Arsenite in Rice (Oryza sativa L.). Ecotoxicol. Environ. Saf. 2017, 138, 47–55. [Google Scholar] [CrossRef] [PubMed]
  44. Manzoor, N.; Ali, L.; Ahmed, T.; Rizwan, M.; Ali, S.; Shahid, M.S.; Schulin, R.; Liu, Y.; Wang, G. Silicon Oxide Nanoparticles Alleviate Chromium Toxicity in Wheat (Triticum aestivum L.). Environ. Pollut. 2022, 315, 120391. [Google Scholar] [CrossRef]
  45. Saidi, I.; Chtourou, Y.; Djebali, W. Selenium Alleviates Cadmium Toxicity by Preventing Oxidative Stress in Sunflower (Helianthus annuus) Seedlings. J. Plant Physiol. 2014, 171, 85–91. [Google Scholar] [CrossRef]
  46. Gill, R.A.; Zang, L.; Ali, B.; Farooq, M.A.; Cui, P.; Yang, S.; Ali, S.; Zhou, W. Chromium-Induced Physio-Chemical and Ultrastructural Changes in Four Cultivars of Brassica napus L. Chemosphere 2015, 120, 154–164. [Google Scholar] [CrossRef]
  47. Singh, V.P.; Srivastava, P.K.; Prasad, S.M. Nitric Oxide Alleviates Arsenic-Induced Toxic Effects in Ridged Luffa Seedlings. Plant Physiol. Biochem. 2013, 71, 155–163. [Google Scholar] [CrossRef]
  48. Wu, Z.; Yin, X.; Bañuelos, G.S.; Lin, Z.Q.; Liu, Y.; Li, M.; Yuan, L. Indications of Selenium Protection against Cadmium and Lead Toxicity in Oilseed Rape (Brassica napus L.). Front. Plant Sci. 2016, 7, 1875. [Google Scholar] [CrossRef] [Green Version]
  49. Tripathi, D.K.; Singh, V.P.; Prasad, S.M.; Chauhan, D.K.; Dubey, N.K. Silicon Nanoparticles (SiNp) Alleviate Chromium (VI) Phytotoxicity in Pisum sativum (L.) Seedlings. Plant Physiol. Biochem. 2015, 96, 189–198. [Google Scholar] [CrossRef]
  50. Riaz, M.; Kamran, M.; Rizwan, M.; Ali, S.; Parveen, A.; Malik, Z.; Wang, X. Cadmium Uptake and Translocation: Selenium and Silicon Roles in Cd Detoxification for the Production of Low Cd Crops: A Critical Review. Chemosphere 2021, 273, 129690. [Google Scholar] [CrossRef]
  51. Shinde, S.; Villamor, J.G.; Lin, W.; Sharma, S.; Verslues, P.E. Proline Coordination with Fatty Acid Synthesis and Redox Metabolism of Chloroplast and Mitochondria. Plant Physiol. 2016, 172, 1074–1088. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  52. Nahar, K.; Hasanuzzaman, M.; Alam, M.M.; Fujita, M. Exogenous Glutathione Confers High Temperature Stress Tolerance in Mung Bean (Vigna radiata L.) by Modulating Antioxidant Defense and Methylglyoxal Detoxification System. Environ. Exp. Bot. 2015, 112, 44–54. [Google Scholar] [CrossRef]
  53. Rahman, M.F.; Ghosal, A.; Alam, M.F.; Kabir, A.H. Remediation of Cadmium Toxicity in Field Peas (Pisum sativum L.) through Exogenous Silicon. Ecotoxicol. Environ. Saf. 2017, 135, 165–172. [Google Scholar] [CrossRef]
  54. Kumar, M.; Bijo, A.J.; Baghel, R.S.; Reddy, C.R.K.; Jha, B. Selenium and Spermine Alleviate Cadmium Induced Toxicity in the Red Seaweed Gracilaria Dura by Regulating Antioxidants and DNA Methylation. Plant Physiol. Biochem. 2012, 51, 129–138. [Google Scholar] [CrossRef]
  55. Afzal, S.; Chaudhary, N.; Singh, N.K. Role of Soluble Sugars in Metabolism and Sensing under Abiotic Stress. In Plant Growth Regulators; Springer: Berlin/Heidelberg, Germany, 2021. [Google Scholar]
  56. Mostofa, M.G.; Rahman, M.M.; Ansary, M.M.U.; Fujita, M.; Tran, L.S.P. Interactive Effects of Salicylic Acid and Nitric Oxide in Enhancing Rice Tolerance to Cadmium Stress. Int. J. Mol. Sci. 2019, 20, 579. [Google Scholar] [CrossRef] [Green Version]
  57. Sardar, R.; Ahmed, S.; Shah, A.A.; Yasin, N.A. Selenium Nanoparticles Reduced Cadmium Uptake, Regulated Nutritional Homeostasis and Antioxidative System in Coriandrum Sativum Grown in Cadmium Toxic Conditions. Chemosphere 2022, 287, 132332. [Google Scholar] [CrossRef]
  58. Yang, S.; Ulhassan, Z.; Shah, A.M.; Khan, A.R.; Azhar, W.; Hamid, Y.; Hussain, S.; Sheteiwy, M.S.; Salam, A.; Zhou, W. Salicylic Acid Underpins Silicon in Ameliorating Chromium Toxicity in Rice by Modulating Antioxidant Defense, Ion Homeostasis and Cellular Ultrastructure. Plant Physiol. Biochem. 2021, 166, 1001–1013. [Google Scholar] [CrossRef] [PubMed]
  59. Handa, N.; Kohli, S.K.; Thukral, A.K.; Bhardwaj, R.; Alyemeni, M.N.; Wijaya, L.; Ahmad, P. Protective Role of Selenium against Chromium Stress Involving Metabolites and Essential Elements in Brassica juncea L. Seedlings. 3 Biotech 2018, 8, 66. [Google Scholar] [CrossRef]
  60. Ulhassan, Z.; Khan, I.; Hussain, M.; Khan, A.R.; Hamid, Y.; Hussain, S.; Allakhverdiev, S.I.; Zhou, W. Efficacy of Metallic Nanoparticles in Attenuating the Accumulation and Toxicity of Chromium in Plants: Current Knowledge and Future Perspectives. Environ. Pollut. 2022, 315, 120390. [Google Scholar] [CrossRef] [PubMed]
Sustainability 15 05361 g001 550
Figure 1. Effects of exogenous selenium (Se) (5 μmol L−1) and silicon (Si) (2.5 mmol L−1), individually or in combination, on the contents of chromium in the chromium (Cr) (0, 100 μmol L−1) treated Chinese cabbage. Bars indicate the standard deviation (SD) of the mean (n = 3), and different lowercase letters indicate significant differences among treatments (p < 0.05).
Figure 1. Effects of exogenous selenium (Se) (5 μmol L−1) and silicon (Si) (2.5 mmol L−1), individually or in combination, on the contents of chromium in the chromium (Cr) (0, 100 μmol L−1) treated Chinese cabbage. Bars indicate the standard deviation (SD) of the mean (n = 3), and different lowercase letters indicate significant differences among treatments (p < 0.05).
Sustainability 15 05361 g001
Sustainability 15 05361 g002 550
Figure 2. Effects of exogenous selenium (Se) (5 μmol L−1) and silicon (Si) (2.5 mmol L−1), individually or in combination, on the contents of chlorophyll a (A), chlorophyll b (B), and carotenoid (C) in the chromium (Cr) (0, 100 μmol L−1) treated Chinese cabbage. Bars indicate the standard deviation (SD) of the mean (n = 3), and different lowercase letters indicate significant differences among treatments (p < 0.05).
Figure 2. Effects of exogenous selenium (Se) (5 μmol L−1) and silicon (Si) (2.5 mmol L−1), individually or in combination, on the contents of chlorophyll a (A), chlorophyll b (B), and carotenoid (C) in the chromium (Cr) (0, 100 μmol L−1) treated Chinese cabbage. Bars indicate the standard deviation (SD) of the mean (n = 3), and different lowercase letters indicate significant differences among treatments (p < 0.05).
Sustainability 15 05361 g002
Sustainability 15 05361 g003 550
Figure 3. Effects of exogenous selenium (Se) (5 μmol L−1) and silicon (Si) (2.5 mmol L−1), individually or in combination, on the contents of MDA (A) and H2O2 (B) in the chromium (Cr) (0, 100 μmol L−1) treated Chinese cabbage. Bars indicate the standard deviation (SD) of the mean (n = 3), and different lowercase letters indicate significant differences among treatments (p < 0.05).
Figure 3. Effects of exogenous selenium (Se) (5 μmol L−1) and silicon (Si) (2.5 mmol L−1), individually or in combination, on the contents of MDA (A) and H2O2 (B) in the chromium (Cr) (0, 100 μmol L−1) treated Chinese cabbage. Bars indicate the standard deviation (SD) of the mean (n = 3), and different lowercase letters indicate significant differences among treatments (p < 0.05).
Sustainability 15 05361 g003
Sustainability 15 05361 g004 550
Figure 4. Effects of exogenous selenium (Se) (5 μmol L−1) and silicon (Si) (2.5 mmol L−1), individually or in combination, on the contents of SOD (A), CAT (B), and POD (C) in the chromium (Cr) (0, 100 μmol L−1) treated Chinese cabbage. Bars indicate the standard deviation (SD) of the mean (n = 3), and different lowercase letters indicate significant differences among treatments (p < 0.05).
Figure 4. Effects of exogenous selenium (Se) (5 μmol L−1) and silicon (Si) (2.5 mmol L−1), individually or in combination, on the contents of SOD (A), CAT (B), and POD (C) in the chromium (Cr) (0, 100 μmol L−1) treated Chinese cabbage. Bars indicate the standard deviation (SD) of the mean (n = 3), and different lowercase letters indicate significant differences among treatments (p < 0.05).
Sustainability 15 05361 g004
Sustainability 15 05361 g005 550
Figure 5. Effects of exogenous selenium (Se) (5 μmol L−1) and silicon (Si) (2.5 mmol L−1), individually or in combination, on the contents of proline (A) and Gsh (B) in the chromium (Cr) (0, 100 μmol L−1) treated Chinese cabbage. Bars indicate the standard deviation (SD) of the mean (n = 3), and different lowercase letters indicate significant differences among treatments (p < 0.05).
Figure 5. Effects of exogenous selenium (Se) (5 μmol L−1) and silicon (Si) (2.5 mmol L−1), individually or in combination, on the contents of proline (A) and Gsh (B) in the chromium (Cr) (0, 100 μmol L−1) treated Chinese cabbage. Bars indicate the standard deviation (SD) of the mean (n = 3), and different lowercase letters indicate significant differences among treatments (p < 0.05).
Sustainability 15 05361 g005
Sustainability 15 05361 g006 550
Figure 6. Effects of exogenous selenium (Se) (5 μmol L−1) and silicon (Si) (2.5 mmol L−1), individually or in combination, on soluble protein (A) and soluble sugar (B) in the chromium (Cr) (0, 100 μmol L−1) treated Chinese cabbage. Bars indicate the standard deviation (SD) of the mean (n = 3), and different lowercase letters indicate significant differences among treatments (p < 0.05).
Figure 6. Effects of exogenous selenium (Se) (5 μmol L−1) and silicon (Si) (2.5 mmol L−1), individually or in combination, on soluble protein (A) and soluble sugar (B) in the chromium (Cr) (0, 100 μmol L−1) treated Chinese cabbage. Bars indicate the standard deviation (SD) of the mean (n = 3), and different lowercase letters indicate significant differences among treatments (p < 0.05).
Sustainability 15 05361 g006
Sustainability 15 05361 g007 550
Figure 7. Principal component analysis (PCA) biplot, PC 1 and 2, showing the relationship between the examined variables and of different treatments. The direction of the arrows shows the correlations of variables with given PCs.
Figure 7. Principal component analysis (PCA) biplot, PC 1 and 2, showing the relationship between the examined variables and of different treatments. The direction of the arrows shows the correlations of variables with given PCs.
Sustainability 15 05361 g007
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Fu, X.; Mehmood, S.; Ahmed, W.; Ou, W.; Suo, P.; Zhang, Q.; Fu, X.; Sun, Z.; Li, W. Reducing Chromium Toxicity in Chinese Cabbage through Synergistic Effects of Silicon and Selenium: A Study of Plant Growth, Chromium Content, and Biochemical Parameters. Sustainability 2023, 15, 5361. https://doi.org/10.3390/su15065361

AMA Style

Fu X, Mehmood S, Ahmed W, Ou W, Suo P, Zhang Q, Fu X, Sun Z, Li W. Reducing Chromium Toxicity in Chinese Cabbage through Synergistic Effects of Silicon and Selenium: A Study of Plant Growth, Chromium Content, and Biochemical Parameters. Sustainability. 2023; 15(6):5361. https://doi.org/10.3390/su15065361

Chicago/Turabian Style

Fu, Xiuxian, Sajid Mehmood, Waqas Ahmed, Wenjie Ou, Penghui Suo, Qinwen Zhang, Xiuhao Fu, Zhongyi Sun, and Weidong Li. 2023. "Reducing Chromium Toxicity in Chinese Cabbage through Synergistic Effects of Silicon and Selenium: A Study of Plant Growth, Chromium Content, and Biochemical Parameters" Sustainability 15, no. 6: 5361. https://doi.org/10.3390/su15065361

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop