Next Article in Journal
Bioassessment of Phylogenetic Relatedness and Plant Growth Enhancement of Endophytic Bacterial Isolates from Cowpea (Vigna unguiculata) Plant Tissues
Previous Article in Journal
Polyploid Induction and Karyotype Analysis of Dendrobium officinale
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Horticulturae
Volume 9
Issue 3
10.3390/horticulturae9030330
horticulturae-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

Exploring Effects of Exogenous Selenium on the Growth and Nutritional Quality of Cabbage (Brassica oleracea var. capitata L.)

by
Li Yu
1,†,
Qiangwen Chen
1,2,†,
Xiaoli Liao
1,
Xiaoyan Yang
3,
Wei Chao
1,
Xin Cong
2,4,
Weiwei Zhang
1,
Yongling Liao
1,
Jiabao Ye
1,
Hua Qian
5,
Yang Zhao
5,
Shuiyuan Cheng
4,* and
Feng Xu
1,*
1
College of Horticulture and Gardening, Yangtze University, Jinzhou 434025, China
2
Enshi Se-Run Material Engineering Technology Co., Ltd., Enshi 445000, China
3
Henry Fok School of Biology and Agricultural, Shaoguan University, Shaoguan 512005, China
4
National R&D Center for Se-Rich Agricultural Products Processing, School of Modern Industry for Selenium Science and Engineering, Wuhan Polytechnic University, Wuhan 430023, China
5
Heilongjiang Academy of Agricultural Sciences, Harbin 150086, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Horticulturae 2023, 9(3), 330; https://doi.org/10.3390/horticulturae9030330
Submission received: 16 January 2023 / Revised: 25 February 2023 / Accepted: 27 February 2023 / Published: 2 March 2023
Browse Figures
Review Reports Versions Notes

Abstract

:
Selenium (Se) is an important trace element in human and animal health. Approximately 0.5–1 billion people worldwide are facing Se deficiency which can result in various endemic diseases. Cabbage is one of the most popular vegetables and can accumulate Se through biofortification. Therefore, producing Se-enriched cabbage may be an effective method to alleviate Se deficiency. In this study, the effects of different concentrations of selenite application on the growth and nutritional quality of cabbage were investigated and the results showed that the growth of cabbage was promoted at low concentrations of selenite (0.1–0.4 mmol/L) but inhibited at high concentrations (0.8–1.6 mmol/L). Concentrations of 0.1–0.2 mmol/L of selenite induced the accumulation of primary metabolites (soluble proteins, soluble sugars, and free amino acids), representative secondary metabolites (ascorbic acid, glucosinolates, flavonoids, anthocyanins, and phenolic acids), and important antioxidant enzyme (glutathione peroxidase, catalase, and superoxide dismutase) activity to improve the nutritional quality of cabbages. In addition, a higher concentration (0.8–1.6 mmol/L) of selenite proved beneficial in the accumulation of total Se and representative organic Se in cabbages. The main organic Se species in cabbage were selenomethionine (SeMet), accounting for 12.10% of total Se, followed by selenocysteine (SeCys2), accounting for 2.96% of total Se. It is suggested that an appropriate dose of exogenous selenite could be selected for different production purposes in cabbage cultivation. These findings are helpful for us to deeply understand the effects of selenite on the growth and nutritional quality of cabbages and to provide reliable technical support for vegetable cultivation and Se biofortification.

1. Introduction

Selenium (Se) is an indispensable element for human and animal health. It is involved in immune regulation, thyroid hormone metabolism, and cancer prevention [1,2,3]. However, approximately 0.5–1 billion people worldwide are facing the threat of Se deficiency [4]. Previous studies, such as Keshan and Kashin-Beck [5], have found that Se deficiency can lead to several diseases. Therefore, supplementary Se for humans is extremely necessary with a daily recommended intake of 50–200 μg [6]. Plants are an important source of dietary Se, but the content of Se in plants is too low to meet the need of humans. A growing number of researchers, in recent years, have considered obtaining Se-enriched food through biofortification to solve this problem [7]. For instance, compared with a control group, selenate-treated Cardamine violifolia contained more than 7475.95 mg/kg dry weight of Se in its leaves with about 90% of it organic Se, mainly in SeCys2 forms [8]. Besides, Se biofortification can also affect nutritional quality and secondary metabolites such as soluble sugar, amino acids, and flavonoids [9]. For example, selenite treatment can significantly increase soluble sugar content but inhibit free amino acid accumulation in Brassica oleracea L. var. italica [4]. The content of flavonoids increased under 100 μ mol/L of selenite treatment in three varieties of broccoli [10]. Therefore, Se biofortification may be a feasible way to alleviate the phenomenon of Se insufficiency in humans in the long-term perspective.
In the environment, selenite and selenate are mainly inorganic Se species. Compared to selenate, selenite has low toxicity and a high organic Se conversion rate and is converted directly into selenide without ATP sulfurylase catalysis [11,12]. Selenite is absorbed by plants through silicon influx transporters and phosphate transporters [13]. Subsequently, most of the absorbed selenite can be converted into organic Se in the roots, and a little is transported to the shoots [14]. For instance, after root application of selenite in Oryza sativa L, the contents of SeMet in the roots and shoots were 5.94 ± 0.06 and 3.10 ± 0.15, respectively [15]. However, the selenite absorption and conversion processes remain unclear and need further investigation.
Cabbage belongs to the Cruciferae family and is rich in nutritional substances such as vitamins, minerals, and secondary metabolites (e.g., phenolic acid, carotenoid, and glucosinolate) [16]. Cruciferae vegetables are interesting as they accumulate Se compounds [17]. For example, studies on broccoli found that selenium yeast and sodium selenite significantly increased the organic Se content [4]. Hence, in this study, cabbage was selected as the experimental material and selenite was used as the source of Se as it is cheaper and less toxic than selenate. Soil application using different concentrations of selenite was performed, and plant growth, nutritional quality, total Se content, Se specification, secondary metabolic substance, and antioxidant enzyme activity were determined. In brief, the primary purpose of our experiments was to screen for the suitable Se concentration for cabbage growth and provide a theoretical and technical foundation for Se-enriched agricultural production.

2. Materials and Method

2.1. Plant Materials and Treatment

The experiments were carried out at the Yangtze University farm (77° E latitude and 112° E longitude) and the cabbage seed (Brassica oleracea var. capital L.cv ‘chunfeng’) obtained from the vegetable institute of Jiangsu Academy of Agricultural Science, China, was a hybrid species of Chicken heart and Jin zaosheng. Cabbage seeds were sown into hole trays and then placed in a light incubator with a temperature of 16 ± 1 °C and relative humidity of 75%. The photoperiod was 14 h of light with an intensity of 240 µmol/m2 s. Seedlings with 6–7 true leaves were transplanted into plastic pots (diameter, 23.5 cm, height, 14 cm) that contained 3.5 kg mixture of soil and vegetable seedling substrates (ratio: 4:1) (pH 7.5 and an Se content of 1.37 mg/kg DW) and subsequently placed in the greenhouse of Yangtze University at 20 °C and 60% relative humidity. Then, the nitrogen (Urea) and phosphorus (Potassium dihydrogen phosphate) fertilizer utilization was set at 73.53 mg/kg and 23.97 mg/kg, respectively, to support nutrition for cabbage growth. Seven days after transplantation, sodium selenite solution was poured into plastic pots at concentrations of 0, 0.1, 0.2, 0.4, 0.8, and 1.6 mmol/L with a volume of 300 mL. The treatment was conducted every 10 days, a total of 4 times. The experiment was performed with randomized complete block design with three replicates and six plants per treatment. The cabbage roots, heads, and leaves were harvested 120 days after treatment. The samples were immediately frozen in liquid nitrogen and stored in a −80 °C refrigerator for further study.

2.2. Determination of Total Selenium and Sulfur

The content of total Se in cabbage was determined by liquid chromatography–atomic fluorescence spectrometry (LC-AFS8510, Beijing, Haiguang, China) using the following instrument parameters: lamp current 80 mA, negative high voltage 330 V, and inject volume 0.1 mL. Se standard (1000 μg/mL) purchased from the Chinese Academy of Metrology and diluted into different concentrations to construct the standard curve. Samples were pretreated according to the method of Xia et al. [18]. The cabbage head part was oven-dried at 65 °C to a constant weight and ground to powder using a grinder (IKA, A11, Staufen City, Germany). The powder was stored in a self-sealing bag to further analyze total Se, Se form, and total sulfur content. The cabbage sample was digested according to the method of Rao et al. with minor modifications [19]. In brief, an approximately 0.5 g cabbage sample was accurately weighed. Next, 10 mL HNO3 and 5 mL H2O2 were added to the digestion tube for microwave digestion treatment (YMW 40, Yong Le Kang Instrument, Changsha City, China). A quantity of 5 mL of 6 mol/L HCl was added to the digestion tube after digestion and the mixture was transferred into a graphite digester (YKM20, Yong Le Kang Instrument, Changsha City, China) and heated until transparent. Then, 2.5 mL of K3[Fe (CN)6] was added to the centrifuge tube and the solution was adjusted to 10 mL for total Se detection. The total sulfur content was measured using a CLS-3000 Coulomb instrument (Jiangsu Guochuang Analytical Instrument, China) in accordance with the method of Wilkin [20].

2.3. Detection of Se Species in Cabbage

Se species in cabbage head were measured by liquid chromatography-atomic fluorescence spectrometry (LC-AFS). SeCys2 (selenocysteine), SeMeCys (Se-methyl selenocysteine), Se IV (selenite), SeMet (selenomethionine), and Se VI (selenate) were purchased from the Center of National Standard Substances (Beijing, China). The solutions were diluted into different concentrations for standard curve construction. About 0.3 g of cabbage head powder was mixed with 5 mL protease XIV (8 mg/mL, pH 7.8) and incubated at 37 °C at 200 rpm for 16 h in an orbital shaker (ZQZY-75BN, Zhi Cu instrument, China). Then, the samples were centrifuged at 12,000 rpm at 4 ℃ for 10 min and the supernatant was collected and filtered through a 0.22 μm mixed cellulose nitrate membrane for detection. The instrument parameters were set as follows: negative high voltage, 320 V; inject volume, 0.1 mL; flow rate carrier gas, 600 mL/min; main current, 80 V; and chromatographic column, PRP-X100 μm 250 × 2.1 mm; mobile phase 20 mmol/L KCl + 40 mmol/L KH2PO4 (pH 6).

2.4. Determination of Soluble Protein, Soluble Sugar, Free Amino Acid, and Chlorophyll Content

Soluble protein in the cabbages was measured using the Coomassie Brilliant Blue G-250 dye method [21]. Soluble sugar was determined according to the method of Ulhassan [22]. The free amino acid content was determined using the method of Shu [23]. In addition, chlorophyll content was measured using ultraviolet spectrophotometry and detected at 663 and 645 nm. Every treatment group contained three biological and technical replicates. Briefly, approximately 0.5 g of a fresh cabbage sample was weighed into a mortar and ground into homogenate; then, 5 mL of 95% ethanol was added until the tissue turned white. The extracts were filtered using a funnel with filter paper into 10 mL brown bottles, then marked to the volume with 95% ethanol.

2.5. Detection of Ascorbic Content, Glucosinolate, Flavonoid, Anthocyanin, and Phenolic Acid

The ascorbic acid content in fresh cabbage heads was determined via 2,6-dichlorophenol indophenol [24]. The total glucosinolate content of cabbage was determined using a glucose oxidase/prostatic acid phosphatase kit (Solarbio Life Sciences, Beijing, China). In the control group, 2.8 mL of acidified methanol (40% methanol and 0.5% acetic acid) was added to 0.50 g of a powdered fresh cabbage sample. In the experimental group, acidified methanol was instead added to deionized water and subsequently incubated in a water bath for 10 min at 37 °C. A 2.1 mL quantity of 100% methanol and 2 mg of activated carbon were added to stop the reaction. All samples were centrifuged at 13,000× g for 10 min at 4 °C, and the glucose content in the supernatant was detected using a glucose kit. Total glucosinolate content in the cabbage was calculated as the difference in glucose content between the experimental and control group [10]. The total flavonoid content of the cabbage was determined by the sodium nitrite-aluminum nitrate colorimetric method and detected at 510 nm [10]. Anthocyanin content was determined using a UV spectrophotometer. About 0.05 g of dry cabbage head powder was added to 2 mL of 0.1% methanol and extracted at 4 °C for 24 h in the dark. The mixture was centrifuged at 12,000 rpm for 12 min, and the supernatant was collected. 500 μL of supernatant was added into a 1.5 mL centrifuge tube with the addition of 500 μL of chloroform and detected at 530 nm. The total phenolic acid content was determined according to the method of Margraf with minor modifications [25]. In brief, 0.5 g tissue samples were soak-extracted in 20 mL of 50% ethanol at room temperature for 30 min and then centrifuged at 5000 rpm for 10 min. The supernatant was collected and detected at 720 nm.

2.6. Determination of Antioxidant Enzyme Activity

Fresh cabbage head (0.5 g) was ground into powder with liquid nitrogen and dissolved in 5 mL of phosphate buffer (0.05 M, pH 7.8). The mixture was centrifuged at 1000 rpm for 10 min, and the supernatant was collected. The activities of catalase (CAT), peroxidase (POD), and superoxide dismutase (SOD) were detected using the corresponding assay kits according to the manufacturer’s instructions (Nanjing JianCheng Bioengineering Institute, Nanjing, China). The activity of glutathione peroxidase (GPX) in the cabbage head was determined using a cellular GPX assay kit with NADPH (Beyotime Biotechnology, Shanghai, China).

2.7. Statistical Analysis

Data were analyzed using Origin (Origin Lab, Northampton, MA, USA) software [26]. All results are represented as mean values ± standard deviations. Results were considered significant when the p < 0.05. All experiments were performed in biological and technical triplicates.

3. Results

3.1. Effects of Selenite on the Growth of Cabbage

The growth parameters of cabbage treated with different concentrations of sodium selenite and the results are shown in Figure 1 and Table 1. The head size of cabbages initially increased and then decreased, reaching a peak value at 0.4 mmol/L, which is about 31.05% higher than those in the control group. Although 1.6 mmol/L sodium selenite treatment significantly inhibited the head weight of cabbages, 0.1 to 0.8 mmol/L selenite treatment showed a positive stimulatory effect. Moreover, 0.4 mmol/L selenite treatment significantly promoted cabbage growth compared to the control group. However, 0.8 mmol/L and 1.6 mmol/L of selenite reduced the total plant weight of cabbage by 1.15% and 16.20%, respectively.

3.2. Effects of Selenite Treatments on Total Se, Sulfur, and Se Species Content of Cabbage

The total Se content of cabbage heads showed a constantly increasing trend. Furthermore, it increased by 2.43, 2.72, 6.25, 10.56, and 22.66-fold, compared to the control group (Figure 2A). Se and sulfur have similar chemical properties, so we evaluated the total sulfur content of cabbages to determine the relationship between Se and sulfur in the sample cabbages. The results showed no significant difference in the variation of sodium selenite dose (Figure 2B).

3.3. Effect of Different Concentration Selenite Treatments on Se Speciation of Cabbage

Se species were determined by LC-AFS, and the results are shown in Table 2. Low amounts of SeMet and SeO42− were detected after 0.4 mmol/L selenite treatment, which reached 3.37 and 0.87 μg/g drought weight (DW), respectively. Additionally, five Se species (e.g., SeCys2, SeMeCys, SeMet SeO32− and SeO42−) were detected after 0.8 and 1.6 mmol/L treatments and accounted for 6.65%, 8.92%, 0.91%, 3.93%, 2.06%, 10.98%, 0.16%, 0.20%, and 3.10% of the total Se content.

3.4. Effects of Selenite Treatment on Soluble Protein, Soluble Sugar, Free Amino Acid, and Chlorophyll Content of Cabbage

The results of soluble protein, soluble sugar, free amino acid, and chlorophyll are shown in Figure 3. The soluble protein content of cabbage heads initially increased and then decreased, reaching a maximum at 0.2 mmol/L (Figure 3A). Compared to the control group, the soluble sugar content initially increased and then decreased. The maximum content was detected at the 0.8 mmol/L treatment and increased by 165.22% (Figure 3B). Curiously, the content of free amino acids was not significantly affected at low concentrations but dramatically increased, especially at 1.6 mmol/L treatment (Figure 3C). Sodium selenite treatment did not affect chlorophyll content at low concentrations but inhibited chlorophyll content at 0.4, 0.8, and 1.6 mmol/L treatments (Figure 3D).

3.5. Total Ascorbic Acid, Glucosinolate, Flavonoid, Anthocyanin, and Phenolic Acid Content of Cabbage

To evaluate the impact of exogenous Se on cabbage heads, ascorbic acid, glucosinolate, flavonoid, anthocyanin, and phenolic acid contents were measured. The results showed that the ascorbic acid content initially increased and then decreased, and the peak value was detected at 0.1 mmol/L (Figure 4A). The total glucosinolate content was increased by 90.38%, 107.95%, 89.54%, 56.07%, and 63.18%, compared to the control group (Figure 4B). The accumulation of flavonoids was significantly promoted between 0.2 and 1.6 mmol/L treatments, but inhibited at 0.1, 0.4, and 0.8 mmol/L treatments (Figure 4C). The anthocyanin content in cabbage heads initially increased and then decreased, reaching the maximum at 0.2 mmol/L (Figure 4D). Moreover, the total phenolic acid content initially increased, then decreased, reaching the maximum at 0.2 mmol/L (Figure 4E).

3.6. Effects of Selenite Treatment on the Antioxidant Enzyme Activity of Cabbage Heads

The activities of GPX, CAT, POD, and SOD were measured, and the results are shown in Figure 5. The results revealed that sodium selenite treatment significantly enhanced the activity of GPX and CAT, which reached the maximum at 0.4 mmol/L treatment (Figure 5A,B). Curiously, the POD activity significantly decreased at 0 to 0.8 mmol/L treatments and was significantly enhanced at 1.6 mmol/L treatment (Figure 5C). The SOD activity was constantly increased at 0.1–0.8 mmol/L treatments and reached a peak value at 1.6 mmol/L treatment (Figure 5D).

4. Discussion

Although Se is not an essential element in higher plants, an appropriate dose of Se can promote the growth of plants and enhance stress resistance [27,28]. From a human perspective, Se supplementation can effectively prevent the occurrence of Keshan and Kashin-Beck diseases. This study found that low concentrations (0.1 and 0.2 mmol/L) of selenite could increase cabbage biomass, including head size, head weight, and total plant weight, but acted as an inhibitor at high concentrations, especially 1.6 mmol/L. This phenomenon has been observed in many plants such as pak choi and cucumber [29,30]. Additionally, similar results were observed when cabbage was treated with different concentrations of selenite [31]. This is probably because low Se concentration could inhibit the production of lipid peroxidation; however, high concentrations resulted in oxidative stress [32].

4.1. Effect of Different Concentrations of Selenite on Total Se Content and Se Species of Cabbage

Our findings indicated that cabbage could accumulate Se, and the total Se and SeMet in cabbage heads increased rapidly with Se treatment (Figure 2A or Table 2). It is implied that cabbage can be used as a raw material for developing Se-rich products. Se is absorbed by plants and then converted into organic Se, such as SeCys2 and SeMet [33,34]. In this study, SeMet was the main organic Se speciation in cabbage, followed by SeCys2 (Table 2). These results are consistent with a report on potato and wheat [12,35]. Besides, a previous study found that selenate was the central speciation in foliar-sprayed cabbage [36], indicating an efficient soil application of high organic Se conversion. In the plants, selenate could be catalyzed by ATP sulfurylase and APS reductase to form selenite (a rate-limiting process), followed by cysteine synthase and methionine synthase to form SeMet [37]. It is speculated that the exogenous selenite was transformed into SeMet through a Se metabolic process in the cabbage heads. A part of SeCys2 was detected in 0.8 and 1.6 mmol/L selenite treatment. Studies on rice found that SeCys2 accumulation may be due to SeMet transformation [38]. In addition, a small amount of SeMeCy was detected at high concentrations of selenite treatment (0.8 and 1.6 mmol/L) (Table 2). Previous research has demonstrated that organic Se, such as MeSeCys, was the main Se species in Se-hyperaccumulation plants, which positively prevents excessive Se incorporation entering proteins and alleviates the toxicity of Se in plants [39]. It is suggested that MeSeCys may enhance the resistance to high concentrations of exogenous sodium selenite to a certain extent in the cabbage heads. Additionally, MeSeCys existing in brassica plants can help with Se accumulation [40]. Therefore, we speculate that the total Se content increase may be caused by this compound.

4.2. Effect of Different Concentrations of Selenite on the Primary Metabolisms of Cabbage

Soluble proteins and sugars are essential for osmotic adjustment in response to stress and are important nutrition indicators for fruits and vegetables [41,42]. Some studies have shown that applying Se to plants, such as tomato, grape, and Ipomoea aquatica, can change soluble protein and sugar [9,43,44]. In the present study, the content of soluble protein was significantly increased in the treatment groups compared to the control group (Figure 3A). Earlier studies found that selenite can replace sulfur in amino acid cysteine and methionine to produce SeMet and SeCys into protein, affecting protein accumulation [45]. Compared to the control group, soluble sugar content significantly increased, especially at 0.8 mmol/L treatment (Figure 3B). Ren et al. found that selenite could modulate the sucrose metabolism enzyme activity and affect the synthesis of soluble sugar [46]. The change of soluble sugar in our study may be associated with the increasing activity of sucrose metabolism enzymes. However, further studies are required to confirm this hypothesis. In addition, this study found that low-concentration selenite treatment (0.1 and 0.2 mmol/L) could increase the chlorophyll content but was inhibitive at high-concentrations (0.8 and 1.6 mmol/L) (Figure 3D). According to prior literature, low concentrations of Se could promote the synthesis of a chlorophyll precursor, whereas high concentrations of Se can act as a suppressor [47,48]. Moreover, the content of free amino acids increased with the treatment concentration compared to the control group (Figure 3C). A similar result was obtained by Hu et al. [49]. Se can affect amino acid biosynthesis by enhancing plants’ N accumulation [50]. These substances are essential primary metabolites and provide the necessary precursors for synthesizing secondary metabolites.

4.3. Effect of Different Concentration of Selenite on Ascorbic Acid Glucosinolate Flavonoid Anthocyanin and Phenolic Acid

The ascorbic acid content was significantly increased in our study (Figure 4A) which was consistent with a study of apples [51]. It is reported that ascorbic acid could interact with GPX, thereby preventing cell damage [9]. GPX is also involved in ascorbic acid recycling [52]. Glucosinolates are a class of sulfur-enriched secondary metabolites. Previous researchers found that glucosinolates are unique metabolites in Cruciferae plants, and the accumulation of glucosinolates in plants was affected by Se [53,54]. For example, the glucosinolates content of broccoli was increased under selenite treatment [10]. Se can affect plant glucosinolate accumulation by regulating glucosinolate metabolic pathway gene expression [55]. The physiological results in our research are consistent with the reports on the biofortification of cabbage with Se yeast and selenate as Se sources [10]. Flavonoids have antioxidant activity, vital in resisting abiotic and biotic stresses [56]. In the present study, the flavonoid content was increased, especially at 1.6 mmol/L treatment (Figure 4C). It is speculated that increased flavonoid content helped cabbage alleviate oxidant stress-induced damage caused by excessive Se. Anthocyanin is a water-soluble pigment in various edible vegetables, fruits, and flowers [57]. This study found that low concentrations (0.1 and 0.2 mmol/L) of Se can facilitate the accumulation of anthocyanin, whereas high concentrations of Se has the opposite effect (Figure 4D), consistent with Islam et al.’s study [58]. In addition, the phenolic acid content was increased at low concentrations (0.1 and 0.2 mmol/L) but decreased at high concentrations (0.8 and 1.6 mmol/L) (Figure 4E). Prior literature has demonstrated that Se influences the synthesis of phenolic acid compounds by regulating the activity of the precursor compound phenylalanine [50]. In summary, these results indicate that an appropriate amount of selenite can increase the accumulation of beneficial secondary metabolites and enhance plant resistance to environmental stress.

4.4. Effect of Different Concentrations of Selenite on Antioxidant Enzymes

Plants have evolved complex mechanisms to prevent against oxygen damage, including antioxidant enzymes such as GPX, POD, CAT, and SOD [59]. GPX is a crucial enzyme that can catalyze GSH into oxidized GSH to alleviate the damage of peroxides to cells [51]. POD protects the cell against reactive oxygen species [60]. CAT plays a vital role in the degradation of H2O2 in cells [61]. SOD is a cytoprotective enzyme that catalyzes the dismutation of superoxide anion to H2O2 and O2 [62]. Our data showed that the activity of GPX and CAT first increased and then decreased at a high concentration (1.6 mmol/L) (Figure 5A,B). Previous studies showed that a low concentration of Se can exert antioxidant effects, but high concentrations may cause oxidant stress [63,64]. However, this study found that a low concentration of selenite decreased POD activity, whereas high concentrations showed the opposite effect (Figure 5C). Earlier research suggested that high POD activity can enhance plant resistance to drought and cold [65,66]. It is speculated that the POD activity was enhanced in response to the plant damage caused by a high concentration of selenite. The increase in SOD activity at 1.6 mmol/L selenite treatment may be because of excessive H2O2 accumulation which helps alleviate POD stress (Figure 5D). Therefore, antioxidant enzyme activity is an essential index of nutritional quality, and each enzyme might play differential roles in cabbage response to selenite treatment.

5. Conclusions

In summary, the growth and nutritional quality of cabbage heads under different concentrations of selenite were investigated in this study. The results indicated that a low concentration (0.1–0.4 mmol/L) of selenite improved the growth of cabbage plants. Quantities of 0.1–0.2 mmol/L of selenite induced the accumulation of the primary metabolites (soluble proteins, soluble sugars, and free amino acids), representative secondary metabolites (ascorbic acid, glucosinolates, flavonoids, anthocyanins, and phenolic acids), and the important antioxidant enzyme activity (GSH, CAT, and SOD) to improve the nutritional quality of cabbage heads. Moreover, high concentrations (0.8–1.6 mmol/L) of selenite had an inhibitory effect, but the total Se and organic Se species (SeMet) significantly increased following selenite application. According to these results, 0.8 mmol/L can be selected as the suitable selenite treatment concentration for Se biofortification in cabbages and eating 100–400 g of fresh cabbage per day could allow one to reach the daily average Se intake needed for the human body. Moreover, it is suggested that different concentrations of exogenous selenite could be selected for different production purposes in cabbage cultivation. These findings enhanced our understanding of the effects of selenite on the growth and nutritional quality of cabbage and provided new insights into vegetable cultivation and Se biofortification.

Author Contributions

F.X. and X.Y. provided the idea and revisions of this study. L.Y. performed the draft writing, database analysis, and chart drawing. J.Y. supervised the conduct of the experiment. Q.C. and W.C. helped with the manuscript revision. X.L. performed the example collection and data analysis. W.Z. revised the manuscript. Y.L. designed the framework of the manuscript. H.Q. and Y.Z. revised the manuscript. X.C. and S.C. provided supervision and funding acquisition. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Key Research and Development Program of Hubei Province (No. 2020BBA043).

Data Availability Statement

The data used and presented in this paper are available upon request from the corresponding authors.

Conflicts of Interest

The authors declare that they have no known competing financial interest or personal relationships that could have appeared to influence the work reported in this paper.

References

  1. Fairweather-Tait, S.J.; Bao, Y.; Broadley, M.R.; Collings, R.; Ford, D.; Hesketh, J.E.; Hurst, R. Selenium in Human Health and Disease. Antioxid. Redox Signal. 2011, 14, 1337–1383. [Google Scholar] [CrossRef]
  2. Rayman, M.P. The Importance of Selenium to Human Health. Lancet 2000, 356, 233–241. [Google Scholar] [CrossRef] [Green Version]
  3. Rayman, M.P. Selenium in Cancer Prevention: A Review of the Evidence and Mechanism of Action. Proc. Nutr. Soc. 2005, 64, 527–542. [Google Scholar] [CrossRef] [Green Version]
  4. Gui, J.-Y.; Rao, S.; Gou, Y.; Xu, F.; Cheng, S. Comparative Study of the Effects of Selenium Yeast and Sodium Selenite on Selenium Content and Nutrient Quality in Broccoli Florets (Brassica oleracea L. Var. Italica). J. Sci. Food Agric. 2021, 102, 1707–1718. [Google Scholar] [CrossRef]
  5. Loscalzo, J. Keshan Disease, Selenium Deficiency, and the Selenoproteome. N. Engl. J. Med. 2014, 370, 1756–1760. [Google Scholar] [CrossRef]
  6. Ullah, H.; Liu, G.; Yousaf, B.; Ali, M.U.; Irshad, S.; Abbas, Q.; Ahmad, R. A Comprehensive Review on Environmental Transformation of Selenium: Recent Advances and Research Perspectives. Environ. Geochem. Health 2019, 41, 1003–1035. [Google Scholar] [CrossRef]
  7. Newman, R.; Waterland, N.; Moon, Y.; Tou, J.C. Selenium Biofortification of Agricultural Crops and Effects on Plant Nutrients and Bioactive Compounds Important for Human Health and Disease Prevention—A Review. Plant Foods Hum. Nutr. 2019, 74, 449–460. [Google Scholar] [CrossRef]
  8. Wu, M.; Cong, X.; Li, M.; Rao, S.; Liu, Y.; Guo, J.; Zhu, S.; Chen, S.; Xu, F.; Cheng, S.; et al. Effects of Different Exogenous Selenium on Se Accumulation, Nutrition Quality, Elements Uptake, and Antioxidant Response in the Hyperaccumulation Plant Cardamine violifolia. Ecotoxicol. Environ. Saf. 2020, 204, 111045. [Google Scholar] [CrossRef]
  9. Zhu, Z.; Zhang, Y.; Liu, J.; Chen, Y.; Zhang, X. Exploring the Effects of Selenium Treatment on the Nutritional Quality of Tomato Fruit. Food Chem. 2018, 252, 9–15. [Google Scholar] [CrossRef]
  10. Tian, M.; Xu, X.; Liu, Y.; Xie, L.; Pan, S. Effect of Se Treatment on Glucosinolate Metabolism and Health-Promoting Compounds in the Broccoli Sprouts of Three Cultivars. Food Chem. 2016, 190, 374–380. [Google Scholar] [CrossRef]
  11. Pilon-Smits, E.A.; Hwang, S.; Mel Lytle, C.; Zhu, Y.; Tai, J.C.; Bravo, R.C.; Chen, Y.; Leustek, T.; Terry, N. Overexpression of ATP Sulfurylase in Indian Mustard Leads to Increased Selenate Uptake, Reduction, and Tolerance. Plant Physiol. 1999, 119, 123–132. [Google Scholar] [CrossRef] [Green Version]
  12. Zhang, H.; Zhao, Z.; Zhang, X.; Zhang, W.; Huang, L.; Zhang, Z.; Yuan, L.; Liu, X. Effects of Foliar Application of Selenate and Selenite at Different Growth Stages on Selenium Accumulation and Speciation in Potato (Solanum tuberosum L.). Food Chem. 2019, 286, 550–556. [Google Scholar] [CrossRef]
  13. Zhao, X.Q.; Mitani, N.; Yamaji, N.; Shen, R.F.; Ma, J.F. Involvement of Silicon Influx Transporter OsNIP2;1 in Selenite Uptake in Rice. Plant Physiol. 2010, 153, 1871–1877. [Google Scholar] [CrossRef] [Green Version]
  14. Li, H.F.; McGrath, S.P.; Zhao, F.J. Selenium Uptake, Translocation and Speciation in Wheat Supplied with Selenate or Selenite. New Phytol. 2008, 178, 92–102. [Google Scholar] [CrossRef]
  15. Wang, K.; Wang, Y.; Li, K.; Wan, Y.; Wang, Q.; Zhuang, Z.; Guo, Y.; Li, H. Uptake, Translocation and Biotransformation of Selenium Nanoparticles in Rice Seedlings (Oryza sativa L.). J. Nanobiotechnol. 2020, 18, 103. [Google Scholar] [CrossRef]
  16. Vasanthi, H.R.; Mukherjee, S.; Das, D.K. Retraction Notice to: Potential Health Benefits of Broccoli- A Chemico-Biological Overview. Mini-Rev. Med. Chem. 2021, 21, 1796. [Google Scholar] [CrossRef]
  17. Yuan, L.; Zhu, Y.; Lin, Z.; Banuelos, G.; Li, W.; Yin, X. A Novel Selenocystine-Accumulating Plant in Selenium-Mine Drainage Area in Enshi, China. PLoS ONE 2013, 8, e65615. [Google Scholar] [CrossRef]
  18. Xia, Q.; Yang, Z.; Shui, Y.; Liu, X.; Chen, J.; Khan, S.; Wang, J.; Gao, Z. Methods of Selenium Application Differentially Modulate Plant Growth, Selenium Accumulation and Speciation, Protein, Anthocyanins and Concentrations of Mineral Elements in Purple-Grained Wheat. Front. Plant Sci. 2020, 11, 1114. [Google Scholar] [CrossRef]
  19. Rao, S.; Yu, T.; Cong, X.; Xu, F.; Lai, X.; Zhang, W.; Liao, Y.; Cheng, S. Integration Analysis of PacBio SMRT- and Illumina RNA-Seq Reveals Candidate Genes and Pathway Involved in Selenium Metabolism in Hyperaccumulator Cardamine violifolia. BMC Plant Biol. 2020, 20, 492. [Google Scholar] [CrossRef]
  20. Wilkin, R.T.; Bischoff, K.J. Coulometric Determination of Total Sulfur and Reduced Inorganic Sulfur Fractions in Environmental Samples. Talanta 2006, 70, 766–773. [Google Scholar] [CrossRef]
  21. Bradford, M.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]
  22. Ulhassan, Z.; Gill, R.A.; Ali, S.; Mwamba, T.M.; Ali, B.; Wang, J.; Huang, Q.; Aziz, R.; Zhou, W. Dual Behavior of Selenium: Insights into Physio-Biochemical, Anatomical and Molecular Analyses of Four Brassica napus Cultivars. Chemosphere 2019, 225, 329–341. [Google Scholar] [CrossRef]
  23. Shu, S.; Tang, Y.; Yuan, Y.; Sun, J.; Zhong, M.; Guo, S. The Role of 24-Epibrassinolide in the Regulation of Photosynthetic Characteristics and Nitrogen Metabolism of Tomato Seedlings under a Combined Low Temperature and Weak Light Stress. Plant Physiol. Biochem. 2016, 107, 344–353. [Google Scholar] [CrossRef]
  24. Wang, Q.; Peng, C.; Shi, L.; Liu, Z.; Zhou, D.; Meng, H.; Zhao, H.; Li, F.; Zhang, M. A Technical System for the Large-Scale Application of Metabolites from Paecilomyces Variotii SJ1 in Agriculture. Front. Bioeng. Biotechnol. 2021, 9, 671879. [Google Scholar] [CrossRef]
  25. Margraf, T.; Karnopp, A.R.; Rosso, N.D.; Granato, D. Comparison between Folin-Ciocalteu and Prussian Blue Assays to Estimate the Total Phenolic Content of Juices and Teas Using 96-Well Microplates. J. Food Sci. 2015, 80, C2397–C2403. [Google Scholar] [CrossRef]
  26. Ratnayake, K.; Payton, J.L.; Meger, M.E.; Godage, N.H.; Gionfriddo, E.; Karunarathne, A. Blue Light-Triggered Photochemistry and Cytotoxicity of Retinal. Cell Signal. 2020, 69, 109547. [Google Scholar] [CrossRef]
  27. Luo, Y.; Wei, Y.; Sun, S.; Wang, J.; Wang, W.; Han, D.; Shao, H.; Jia, H.; Fu, Y. Selenium Modulates the Level of Auxin to Alleviate the Toxicity of Cadmium in Tobacco. Int. J. Mol. Sci. 2019, 20, 3772. [Google Scholar] [CrossRef] [Green Version]
  28. Liu, Q.; Wang, D.J.; Jiang, X.J.; Cao, Z.H. Effects of the Interactions between Selenium and Phosphorus on the Growth and Selenium Accumulation in Rice (Oryza sativa). Environ. Geochem. Health 2004, 26, 325–330. [Google Scholar] [CrossRef]
  29. Hawrylak-Nowak, B.; Matraszek, R.; Pogorzelec, M. The Dual Effects of Two Inorganic Selenium Forms on the Growth, Selected Physiological Parameters and Macronutrients Accumulation in Cucumber Plants. Acta Physiol. Plant. 2015, 37, 41. [Google Scholar] [CrossRef] [Green Version]
  30. Li, J.; Liang, D.; Qin, S.; Feng, P.; Wu, X. Effects of Selenite and Selenate Application on Growth and Shoot Selenium Accumulation of Pak Choi (Brassica chinensis L.) during Successive Planting Conditions. Environ. Sci. Pollut. Res. Int. 2015, 22, 11076–11086. [Google Scholar] [CrossRef]
  31. Yang, X.; Liao, X.; Yu, L.; Rao, S.; Chen, Q.; Zhu, Z.; Cong, X.; Zhang, W.; Ye, J.; Cheng, S.; et al. Combined Metabolome and Transcriptome Analysis Reveal the Mechanism of Selenate Influence on the Growth and Quality of Cabbage (Brassica oleracea Var. capitata L.). Food Res. Int. 2022, 111135. [Google Scholar] [CrossRef]
  32. Hartikainen, H.; Xue, T.; Piironen, V. Selenium as an Anti-Oxidant and pro-Oxidant in Ryegrass. Plant Soil 2000, 225, 193–200. [Google Scholar] [CrossRef]
  33. Bañuelos, G.S.; Lin, Z.Q.; Wu, L.; Terry, N. Phytoremediation of Selenium-Contaminated Soils and Waters: Fundamentals and Future Prospects. Re.v Environ. Health 2002, 17, 291–306. [Google Scholar] [CrossRef]
  34. Hossain, A.; Skalicky, M.; Brestic, M.; Maitra, S.; Sarkar, S.; Ahmad, Z.; Vemuri, H.; Garai, S.; Mondal, M.; Bhatt, R.; et al. Selenium Biofortification: Roles, Mechanisms, Responses and Prospects. Molecules 2021, 26, 881. [Google Scholar] [CrossRef]
  35. Wang, M.; Ali, F.; Wang, M.; Dinh, Q.T.; Zhou, F.; Bañuelos, G.S.; Liang, D. Understanding Boosting Selenium Accumulation in Wheat (Triticum aestivum L.) Following Foliar Selenium Application at Different Stages, Forms, and Doses. Environ. Sci. Pollut. Res. Int. 2020, 27, 717–728. [Google Scholar] [CrossRef]
  36. Slekovec, M.; Goessler, W. Accumulation of Selenium in Natural Plants and Selenium Supplemented Vegetable and Selenium Speciation by HPLC-ICPMS. Chem. Speciat. Bioavailab. 2015, 17, 63–73. [Google Scholar] [CrossRef]
  37. Yu, Q.; Boyanov, M.I.; Liu, J.; Kemner, K.M.; Fein, J.B. Adsorption of Selenite onto Bacillus subtilis: The Overlooked Role of Cell Envelope Sulfhydryl Sites in the Microbial Conversion of Se(IV). Environ. Sci. Technol. 2018. [Google Scholar] [CrossRef]
  38. Dai, Z.; Imtiaz, M.; Rizwan, M.; Yuan, Y.; Huang, H.; Tu, S. Dynamics of Selenium Uptake, Speciation, and Antioxidant Response in Rice at Different Panicle Initiation Stages. Sci. Total Environ. 2019, 691, 827–834. [Google Scholar] [CrossRef]
  39. Sors, T.G.; Martin, C.P.; Salt, D.E. Characterization of Selenocysteine Methyltransferases from Astragalus Species with Contrasting Selenium Accumulation Capacity. Plant J. 2009, 59, 110–122. [Google Scholar] [CrossRef]
  40. Ávila, F.W.; Yang, Y.; Faquin, V.; Ramos, S.J.; Guilherme, L.R.G.; Thannhauser, T.W.; Li, L. Impact of Selenium Supply on Se-Methylselenocysteine and Glucosinolate Accumulation in Selenium-Biofortified Brassica Sprouts. Food Chem. 2014, 165, 578–586. [Google Scholar] [CrossRef]
  41. Hu, L.; Yang, C.; Zhang, L.; Feng, J.; Xi, W. Effect of Light-Emitting Diodes and Ultraviolet Irradiation on the Soluble Sugar, Organic Acid, and Carotenoid Content of Postharvest Sweet Oranges (Citrus sinensis (L.) Osbeck). Molecules 2019, 24, 3440. [Google Scholar] [CrossRef] [Green Version]
  42. Khatkar, D.; Kuhad, M.S. Short-Term Salinity Induced Changes in Two Wheat Cultivars at Different Growth Stages. Biol. Plant. 2000, 43, 629–632. [Google Scholar] [CrossRef]
  43. Guo, X.; Ji, Q.; Rizwan, M.; Li, H.; Li, D.; Chen, G. Effects of Biochar and Foliar Application of Selenium on the Uptake and Subcellular Distribution of Chromium in Ipomoea Aquatica in Chromium-Polluted Soils. Ecotoxicol. Environ. Saf. 2020, 206, 111184. [Google Scholar] [CrossRef]
  44. Zhu, S.; Liang, Y.; An, X.; Kong, F.; Gao, D.; Yin, H. Changes in Sugar Content and Related Enzyme Activities in Table Grape (Vitis vinifera L.) in Response to Foliar Selenium Fertilizer. J. Sci. Food Agric. 2017, 97, 4094–4102. [Google Scholar] [CrossRef]
  45. Van Hoewyk, D. A Tale of Two Toxicities: Malformed Selenoproteins and Oxidative Stress Both Contribute to Selenium Stress in Plants. Ann. Bot. 2013, 112, 965–972. [Google Scholar] [CrossRef] [Green Version]
  46. Ren, G.; Ran, X.; Zeng, R.; Chen, J.; Wang, Y.; Mao, C.; Wang, X.; Feng, Y.; Yang, G. Effects of Sodium Selenite Spray on Apple Production, Quality, and Sucrose Metabolism-Related Enzyme Activity. Food Chem. 2021, 339, 127883–127889. [Google Scholar] [CrossRef]
  47. Babaei, A.; Ranglová, K.; Malapascua, J.R.; Masojídek, J. The Synergistic Effect of Selenium (Selenite, −SeO32−) Dose and Irradiance Intensity in Chlorella cultures. AMB Express 2017, 7, 56. [Google Scholar] [CrossRef] [Green Version]
  48. Feng, R.; Wei, C.; Tu, S. The Roles of Selenium in Protecting Plants against Abiotic Stresses. Environ. Exp. Bot. 2013, 87, 58–68. [Google Scholar] [CrossRef]
  49. Hu, Q.; Pan, G.; Zhu, J. Effect of Selenium on Green Tea Preservation Quality and Amino Acid Composition of Tea Protein. J. Hortic. Sci. Biotechnol. 2001, 76, 344–346. [Google Scholar] [CrossRef]
  50. Puccinelli, M.; Pezzarossa, B.; Rosellini, I.; Malorgio, F. Selenium Enrichment Enhances the Quality and Shelf Life of Basil Leaves. Plants 2020, 9, 801. [Google Scholar] [CrossRef]
  51. Ren, Z.; Chen, C.; Fan, Y.; Chen, C.; He, H.; Wang, X.; Zhang, Z.; Zuo, Z.; Peng, G.; Hu, Y.; et al. Toxicity of DON on GPx1-Overexpressed or Knockdown Porcine Splenic Lymphocytes in Vitro and Protective Effects of Sodium Selenite. Oxid. Med. Cell. Longev. 2019, 2019, 5769752. [Google Scholar] [CrossRef]
  52. Chen, Z.; Young, T.E.; Ling, J.; Chang, S.-C.; Gallie, D.R. Increasing Vitamin C Content of Plants through Enhanced Ascorbate Recycling. Proc. Natl. Acad. Sci. USA 2003, 100, 3525–3530. [Google Scholar] [CrossRef] [Green Version]
  53. Barickman, T.C.; Kopsell, D.A.; Sams, C.E. Selenium Influences Glucosinolate and Isothiocyanates and Increases Sulfur Uptake in Arabidopsis Thaliana and Rapid-Cycling Brassica oleracea. J. Agric. Food Chem. 2013, 61, 202–209. [Google Scholar] [CrossRef] [PubMed]
  54. Halkier, B.A.; Gershenzon, J. Biology and Biochemistry of Glucosinolates. Annu. Rev. Plant Biol. 2006, 57, 303–333. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  55. Tian, M.; Yang, Y.; Ávila, F.W.; Fish, T.; Yuan, H.; Hui, M.; Pan, S.; Thannhauser, T.W.; Li, L. Effects of Selenium Supplementation on Glucosinolate Biosynthesis in Broccoli. J. Agric. Food Chem. 2018, 66, 8036–8044. [Google Scholar] [CrossRef]
  56. Pourcel, L.; Routaboul, J.-M.; Cheynier, V.; Lepiniec, L.; Debeaujon, I. Flavonoid Oxidation in Plants: From Biochemical Properties to Physiological Functions. Trends Plant Sci. 2007, 12, 29–36. [Google Scholar] [CrossRef]
  57. Riaz, R.S.; Elsherif, M.; Moreddu, R.; Rashid, I.; Hassan, M.U.; Yetisen, A.K.; Butt, H. Anthocyanin-Functionalized Contact Lens Sensors for Ocular PH Monitoring. ACS Omega 2019, 4, 21792–21798. [Google Scholar] [CrossRef] [Green Version]
  58. Islam, M.Z.; Park, B.-J.; Kang, H.-M.; Lee, Y.-T. Influence of Selenium Biofortification on the Bioactive Compounds and Antioxidant Activity of Wheat Microgreen Extract. Food Chem. 2020, 309–328, 125763. [Google Scholar] [CrossRef] [PubMed]
  59. Zhao, L.; Hu, Q.; Huang, Y.; Fulton, A.N.; Hannah-Bick, C.; Adeleye, A.S.; Keller, A.A. Activation of Antioxidant and Detoxification Gene Expression in Cucumber Plants Exposed to a Cu(OH)2 Nanopesticide. Environ. Sci. Nano 2017, 4, 1750–1760. [Google Scholar] [CrossRef] [Green Version]
  60. Lüthje, S.; Meisrimler, C.-N.; Hopff, D.; Möller, B. Phylogeny, Topology, Structure and Functions of Membrane-Bound Class III Peroxidases in Vascular Plants. Phytochemistry 2011, 72, 1124–1135. [Google Scholar] [CrossRef]
  61. Azpilicueta, C.E.; Pena, L.B.; Tomaro, M.L.; Gallego, S.M. Modifications in Catalase Activity and Expression in Developing Sunflower Seedlings under Cadmium Stress. Redox Rep. 2008, 13, 40–46. [Google Scholar] [CrossRef] [PubMed]
  62. Huang, H.; Wang, H.; Tong, Y.; Wang, Y. Insights into the Superoxide Dismutase Gene Family and Its Roles in Dendrobium Catenatum under Abiotic Stresses. Plants 2020, 9, 1452. [Google Scholar] [CrossRef] [PubMed]
  63. González-Morales, S.; Pérez-Labrada, F.; García-Enciso, E.L.; Leija-Martínez, P.; Medrano-Macías, J.; Dávila-Rangel, I.E.; Juárez-Maldonado, A.; Rivas-Martínez, E.N.; Benavides-Mendoza, A. Selenium and Sulfur to Produce Allium Functional Crops. Molecules 2017, 22, 558. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  64. Lanza, M.G.D.B.; Silva, V.M.; Montanha, G.S.; Lavres, J.; Pereira de Carvalho, H.W.; Reis, A.R.D. Assessment of Selenium Spatial Distribution Using μ-XFR in Cowpea (Vigna unguiculata (L.) Walp.) Plants: Integration of Physiological and Biochemical Responses. Ecotoxicol. Environ. Saf. 2021, 207, 111216. [Google Scholar] [CrossRef]
  65. Janská, A.; Marsík, P.; Zelenková, S.; Ovesná, J. Cold Stress and Acclimation—What Is Important for Metabolic Adjustment? Plant Biol. 2010, 12, 395–405. [Google Scholar] [CrossRef]
  66. Song, Y.; Li, J.; Liu, M.; Meng, Z.; Liu, K.; Sui, N. Nitrogen Increases Drought Tolerance in Maize Seedlings. Funct. Plant Biol. 2019, 46, 350–359. [Google Scholar] [CrossRef]
Horticulturae 09 00330 g001 550
Figure 1. The phenotype of cabbage under different concentrations of selenite treatment.
Figure 1. The phenotype of cabbage under different concentrations of selenite treatment.
Horticulturae 09 00330 g001
Horticulturae 09 00330 g002 550
Figure 2. Total selenium (A) and sulfur (B) content in the heads of cabbage under different concentrations of selenite treatment. Results were calculated using a one-way ANOVA and Duncan’s test. Bars represent mean values and standard error of three replications; different letters denote significant differences at p < 0.05.
Figure 2. Total selenium (A) and sulfur (B) content in the heads of cabbage under different concentrations of selenite treatment. Results were calculated using a one-way ANOVA and Duncan’s test. Bars represent mean values and standard error of three replications; different letters denote significant differences at p < 0.05.
Horticulturae 09 00330 g002
Horticulturae 09 00330 g003 550
Figure 3. Effect of selenite on the contents of soluble protein (A), soluble sugar (B), free amino acid (C), and chlorophyll (D) in the heads of cabbage. Data were expressed as mean ± standard error of three replicates and the analysis method was Duncan’s test. Different letters denote significant differences at p < 0.05.
Figure 3. Effect of selenite on the contents of soluble protein (A), soluble sugar (B), free amino acid (C), and chlorophyll (D) in the heads of cabbage. Data were expressed as mean ± standard error of three replicates and the analysis method was Duncan’s test. Different letters denote significant differences at p < 0.05.
Horticulturae 09 00330 g003
Horticulturae 09 00330 g004 550
Figure 4. Effect of different concentrations of sodium selenite on the content of total ascorbic acid (A), glucosinolate (B), flavonoid (C), anthocyanin (D), and phenolic acid (E). The bar represents the mean ± standard error of three replicates and the analysis method was Duncan’s test. Different letters denote significant differences at p < 0.05.
Figure 4. Effect of different concentrations of sodium selenite on the content of total ascorbic acid (A), glucosinolate (B), flavonoid (C), anthocyanin (D), and phenolic acid (E). The bar represents the mean ± standard error of three replicates and the analysis method was Duncan’s test. Different letters denote significant differences at p < 0.05.
Horticulturae 09 00330 g004
Horticulturae 09 00330 g005 550
Figure 5. Effect of selenite on the activity of GSH (A), CAT (B), POD (C), and SOD (D) in the heads of cabbage. The data represent the mean ± standard error of three replicates and the analysis method was Duncan’s test. Different letters denote significant differences with p < 0.05.
Figure 5. Effect of selenite on the activity of GSH (A), CAT (B), POD (C), and SOD (D) in the heads of cabbage. The data represent the mean ± standard error of three replicates and the analysis method was Duncan’s test. Different letters denote significant differences with p < 0.05.
Horticulturae 09 00330 g005
Table
Table 1. Head size, head weight, and total plant weight of cabbage under selenite treatments.
Table 1. Head size, head weight, and total plant weight of cabbage under selenite treatments.
Sodium Selenite Concentration (mmol/L)Head Size (cm)Head Weight (g)Total Plant Weight (g)
010.4 ± 0.40 b303.33 ± 60.82 bc539.46 ± 68.47 ab
0.113 ± 0.607 ab375.9 ± 6.95 ab555.46 ± 31.35 ab
0.212.57 ± 0.80 a367.37 ± 20.21 ab573.1 ± 27.70 a
0.413.03 ± 0.63 a424.03 ± 6.38 a603.7 ± 20.70 a
0.811.33 ± 0.60 a352.13 ± 9.81 abc533.27 ± 11.10 ab
1.610.63 ± 0.41 b275.57 ± 6.70 c452.07 ± 21.25 b
Note: The data are displayed with the mean ± SE of three replications using the Duncan’s test analysis method. Different letters indicate a significant difference at p < 0.05.
Table
Table 2. Se speciation in cabbage heads under selenite treatments.
Table 2. Se speciation in cabbage heads under selenite treatments.
Treatment
(mmol/L)		SeCys2
(μg/g DW)		SeMeCys
(μg/g DW)		SeMet
(μg/g DW)		SeO32−
(μg/g DW)		SeO42−
(μg/g DW)
0NDNDNDNDND
0.1NDNDNDNDND
0.2NDNDNDNDND
0.4NDND3.37 ± 0.111 bND0.87 ± 0.019 c
0.81.76 ± 0.009 a0.024 ± 0.002 b2.36 ± 0.102 c0.24 ± 0.009 a1.04 ± 0.027 b
1.61.17 ± 0.068 b0.116 ± 0.005 a6.24 ± 0.163 a0.09 ± 0.004 b1.76 ± 0.012 a
Note: The data are displayed with the mean ± SE of three replications. Different letters indicate a significant difference at p < 0.05 and the analysis method was Duncan’s test. ND: undetected. SeCys2: selenocysteine, SeMeCys: Se-methyl selenocysteine, SeMet: selenomethionine, SeO32−: selenite, SeO42−: selenate.
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

Yu, L.; Chen, Q.; Liao, X.; Yang, X.; Chao, W.; Cong, X.; Zhang, W.; Liao, Y.; Ye, J.; Qian, H.; et al. Exploring Effects of Exogenous Selenium on the Growth and Nutritional Quality of Cabbage (Brassica oleracea var. capitata L.). Horticulturae 2023, 9, 330. https://doi.org/10.3390/horticulturae9030330

AMA Style

Yu L, Chen Q, Liao X, Yang X, Chao W, Cong X, Zhang W, Liao Y, Ye J, Qian H, et al. Exploring Effects of Exogenous Selenium on the Growth and Nutritional Quality of Cabbage (Brassica oleracea var. capitata L.). Horticulturae. 2023; 9(3):330. https://doi.org/10.3390/horticulturae9030330

Chicago/Turabian Style

Yu, Li, Qiangwen Chen, Xiaoli Liao, Xiaoyan Yang, Wei Chao, Xin Cong, Weiwei Zhang, Yongling Liao, Jiabao Ye, Hua Qian, and et al. 2023. "Exploring Effects of Exogenous Selenium on the Growth and Nutritional Quality of Cabbage (Brassica oleracea var. capitata L.)" Horticulturae 9, no. 3: 330. https://doi.org/10.3390/horticulturae9030330

APA Style

Yu, L., Chen, Q., Liao, X., Yang, X., Chao, W., Cong, X., Zhang, W., Liao, Y., Ye, J., Qian, H., Zhao, Y., Cheng, S., & Xu, F. (2023). Exploring Effects of Exogenous Selenium on the Growth and Nutritional Quality of Cabbage (Brassica oleracea var. capitata L.). Horticulturae, 9(3), 330. https://doi.org/10.3390/horticulturae9030330

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