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Article

Effects of Sodium Selenite on the Rhizosphere Environment, Growth, and Physiological Traits of Oilseed Rape (Brassica napus L.)

1
College of Resources and Environment, Shanxi Agricultural University, Taigu 030801, China
2
Key Laboratory of Land Surface Pattern and Simulation, Institute of Geographical Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China
*
Author to whom correspondence should be addressed.
Agronomy 2023, 13(10), 2508; https://doi.org/10.3390/agronomy13102508
Submission received: 27 August 2023 / Revised: 26 September 2023 / Accepted: 26 September 2023 / Published: 28 September 2023
(This article belongs to the Section Plant-Crop Biology and Biochemistry)

Abstract

:
Soil selenium (Se) speciation characteristics and their influence on the Se enrichment pattern and physiological characteristics of oilseed rape are poorly understood. We investigated dynamic changes in rhizosphere soil physicochemical properties, Se uptake and partitioning, biomass, and physiological indices in oilseed rape under five exogenous Se condition levels (0, 1.0, 2.5, 5.0, and 10.0 mg kg−1 Se in sodium selenite) using soil cultivation experiments. The rhizosphere pH and dissolved organic carbon in the soil solution were higher than those of the non-rhizosphere soil solution. The total Se, water-soluble Se, exchangeable Se, and organic Se contents in soils, as well as rapeseed root/leaf Se contents, significantly increased with increasing exogenous Se. Under 2.5 mg kg−1 Se, the biomass of rapeseed roots and leaves increased at the sixth week (82% and 58%) and eighth week (48% and 32%), respectively, reaching the highest level. Applications of 5.0 mg kg−1 Se at 6 and 8 weeks significantly increased the glutathione peroxidase activity (49%/82%), and decreased malondialdehyde content (23%/39%). Canonical correlation and ridge regression analyses showed that Se in the rapeseed roots/leaves significantly and positively correlated with water-soluble Se, exchangeable Se, and organic Se in rhizosphere soil. Overall, moderate-concentration Se soil application benefited oilseed rape growth (optimum = 2.5 mg kg−1 Se). Our findings reveal the response of oilseed rape to soil Se application based on plant growth and physiological traits, rhizospheric soil solution properties, and Se speciation transformation.

1. Introduction

Selenium (Se) is an essential micronutrient for humans that serves as an important component of the antioxidant system and selenoproteins and has a variety of important biological functions, including cancer prevention, hormone metabolism, anti-aging, viral inhibition, and immune regulation [1,2,3]. Inadequate Se intake can cause human health disorders, including diseases related to oxidative stress, reduced fertility and immune function, and an increased risk of cancer [4]. Currently, nearly 15% of the world’s population is at risk of Se deficiency, and approximately 105 million people in China have varying degrees of Se deficiency [5]. With the gradual increase in people’s understanding of the physiological function and biological nutritional role of Se, the development of Se-enriched agricultural products at home and abroad has seen unprecedented development, and bio-nutritional enhancement technology has been increasingly applied to agricultural production [6,7,8].
Although there is still controversy over whether Se is an essential micronutrient for plants, it is deemed a beneficial element that can promote plant growth and improve stress resistance [9]. In recent years, exogenous Se has been widely used in agricultural fields such as rice, wheat, tea, tomato, potato, and pakchoi. Wang et al. [10] showed that a low concentration of sodium selenite promoted filamentous microalga growth by increasing chlorophyll content and antioxidant capacity. In a hydroponics experiment, Pourebrahimi et al. [11] reported that sodium selenate strengthened the enzymatic and non-enzymatic antioxidant systems of strawberries, thereby reducing the malondialdehyde content, neutralizing the effect of salinity stress, and increasing the fruit yield and size. Further, it has been found that Se application can regulate the soil-plant rhizosphere microenvironment. Cai et al. [12] found the increase in Se bioavailability in chromium-contaminated soil planting pak choi was related to a decrease in Se reductase functional genes and an increase in pH. Jiao et al. [13] demonstrated that amendments with Se nanomaterials enhanced the relative abundance of small molecular organic acids in rhizosphere soil and changed the structure of rhizosphere microbial communities, thereby improving nutrient availability and promoting rice growth.
Oilseed rape (Brassica napus L.) is the world’s third-largest oil crop [14]. China is the second-largest oilseed rape-producing country, accounting for 16% of global production [15]. Oilseed rape is a cruciferous plant, and it displays strong enrichment ability for Se. Ebrahimi et al. [16] studied the effects of different types of exogenous Se on the growth and Se absorption and accumulation of oilseed rape and found that the Se content of oilseed rape fruit pods was increased by 3–6 times after applying selenate. In addition, the efficiency of improving Se content in rapeseed with organic Se at the same concentration was lower than that of inorganic Se. Wang et al. [17] studied the effects of Se application on Se contents in different parts of oilseed rape at the maturity stage and found that the proportion of Se transferred from the roots to aboveground parts increased with an increase in soil Se concentration. In another study by Ulhassan et al. [18], the application of 25 µM Se (as selenite) enhanced antioxidant enzyme activities and promoted rapeseed growth. At present, moderate Se application has been successful in increasing Se concentration in oilseed rape and promoting plant growth. The effect of exogenous Se on the soil-rapeseed rhizosphere environment and its speciation transformation process in soil are not well studied. Therefore, it is urgent to systematically explore the effects of exogenous Se on the rhizosphere environment, growth, and physiological traits of oilseed rape (Brassica napus L.).
In the present study, we aimed to: (1) investigate the response of pH and dissolved organic carbon (DOC) of the soil solution and Se speciation in rhizosphere soil with or without Se addition; (2) quantify the effects of Se application on plant growth, Se uptake, and physiological traits; and (3) establish a multiple regression model to predict the Se content of plants. The findings provide a theoretical basis and scientific guidance for rational Se supplementation during oilseed rape production.

2. Materials and Methods

2.1. Experimental Materials and Design

The test soil was collected from the surface layer (0–20 cm) in Yongjia County, Wenzhou, Zhejiang Province, China. The soil at this site is classified as Cambisols [19]. The basic physical and chemical properties of the soil are shown in Table 1. The pH of soil in DI water (1:2.5, w/v) was determined using a pH meter (PHB-4) [20]. The soil electrical conductivity in DI water (1:5, w/v) was measured using a conductivity meter (CT-20) [21]. Concentrations of organic carbon and organic nitrogen were determined with an automatic carbon and nitrogen analyzer [22]. Soil-available Se was determined according to Xu et al. [20]. Briefly, the soil sample was extracted using a 0.1 mol L−1 (pH = 7.0) KH2PO4–K2HPO4 buffer solution. The soil was then air-dried, grounded, and passed through a 2 mm sieve. Chemical fertilizers, including 150 mg N kg−1 dry soil as urea and 30 mg P kg−1 and 75.5 mg K kg−1 as K2HPO4, were applied into the soil and mixed thoroughly. Rape seed (Brassica napus L.) was provided by the Chinese Academy of Agricultural Sciences.
Generally, selenite and selenate were the main application forms for the agronomic biofortification of Se. Previous research has reported that Se content was lower in plants supplemented with selenite compared with selenate treatment, with a greater reduction in biomass production [23,24]. Moreover, selenite was more conducive to the accumulation of Se in grain than selenate [25]. Therefore, selenite was selected for this study. Sodium selenite in the form of a solution was mixed thoroughly with the soil that had been treated with the base fertilizer, and Se was applied to the soil at concentrations of 0, 1.0, 2.5, 5.0, and 10.0 mg kg−1 for a total of five treatment levels. The soil samples from each treatment were allowed to stand in equilibrium for one month [26], during which the soil moisture was maintained at approximately 60% of the field water holding capacity.
The Se-amended soil was air-dried, thoroughly mixed, and passed through a 2 mm sieve prior to the experiment. A cylindrical rhizobag (30 µm of nylon mesh that is 10 cm in diameter and 9 cm in height) was filled with 120 g of Se-amended soil, then placed in the center of a PVC pot (18 cm in diameter and 11 cm in height) filled with 360 g of dry weight of the same soil. In this system, the surfaces of soil both inside and outside the rhizobag were at the same level. The pots were arranged in a completely randomized block design and grown under natural daylight conditions.
Disinfected seeds were evenly sown (10 seeds) in each pot at a depth of 1 cm. After emergence, the seedlings were thinned to 4 per pot, and each treatment was prepared with twelve replications. Soil moisture was maintained at approximately 65% of the field water holding capacity during plant growth.
On the 6th and 8th weeks after seedling emergence, four pots with plants showing relatively uniform growth were selected for each treatment. Each time, approximately 3 g of fresh rape leaf from each pot was first harvested, rinsed with deionized water, blotted, weighed, and immediately frozen in liquid nitrogen or stored at −80 °C for enzyme activity assays. The remaining plants were then collected by cutting the leaves at the soil surface, and the roots were separated from the rhizobag soils. Leaves and roots were washed, blotted, weighed, oven-dried, weighed again, and pulverized to a fine powder for the analysis of Se content. The soil in the rhizobags was collected and regarded as rhizosphere soil. The soil in the pot, 5 mm away from the rhizobag, was collected, mixed, and considered to be non-rhizosphere soil. All of the soil samples were air-dried, ground, sieved through 2 mm, and stored for further analyses.

2.2. Measurement Indicators and Methods

Extraction of soil solution: Twenty grams of soil sample were weighed into a 100-milliliter centrifuge tube, and 50 mL of 0.01 M CaCl2 solution was added and shaken (200 cpm) for 2 h at 25 °C. Moreover, the solution was centrifuged (3000 rpm) for 25 min and filtered through a 0.45 µm needle filter, and the supernatant was collected [27,28] and used to determine the pH and DOC of the soil solution. The soil solution pH and DOC values were measured using a pH meter (PHB-4) and an automatic carbon and nitrogen analyzer (TOC-TN 1200, Thermo Euroglas, Waltham, MA, USA), respectively.
Determination of soil Se content: Soil water-soluble Se (ultrapure water), exchangeable Se (0.1 M KH2PO4–K2HPO4), and organic matter-bound Se (0.1 M NaOH) were extracted sequentially by the continuous leaching method as previously described [29]. Total Se in the soil was digested by HNO3–HClO4 (5:2), while Se in the plants was digested by HNO3–HClO4 (9:1). The Se content was determined by hydride generation-atomic fluorescence spectrometry (HG-AFS) using a dual-channel atomic fluorescence instrument (AFS 9780, Beijing Haikuang Instrument Co., Ltd., Beijing, China), with a limit of detection of 0.02 ng/mL and a precision (RSD) of 1.0%.
Glutathione peroxidase (GPx) activity was determined using the NADPH oxidation method, and malondialdehyde (MDA) content was determined using the thiobarbituric acid method. Each biochemical index was determined in strict accordance with the instructions of specific kits purchased from Suzhou Keming Biotechnology Co., Ltd., Suzhou, China.

2.3. Data Analyses

Statistical analyses were conducted using the SPSS 25.0 software program (SPSS, Inc., Chicago, IL, USA). The differences in biochemical parameters in soils and plants between the treatments were determined using one-way analyses of variance (ANOVA) followed by Duncan’s test. All tests for significance were two-sided, and p < 0.05 was considered statistically significant. The data reported in this paper are presented as mean values ± standard deviations of four replicates and were plotted with SigmaPlot 12.0 (Systat Software Inc., Chicago, IL, USA).

3. Results

3.1. Effect of Exogenous Se Application on Soil Solution Properties

3.1.1. Soil Solution pH

Figure 1 shows the variation in pH of the rhizosphere and non-rhizosphere soil solutions of oilseed rape at different periods. The pH of the rhizosphere soil solution was higher than that of the non-rhizosphere soil in all cases. At 6 weeks of seedling emergence of oilseed rape, the pH of the rhizosphere soil solution was 4.31–4.56, which was 0.04–0.24 units higher than that of the non-rhizosphere soil solution. By 8 weeks of seedling emergence, the pH of the rhizosphere soil solution continued to increase and maintained a range of 4.33–4.66, with an average increase of 0.04 units relative to that at 6 weeks.

3.1.2. Soil Solution DOC

Figure 2 shows the changes in DOC in the rhizosphere and non-rhizosphere soil solutions at different periods. The DOC of the rhizosphere soil solution tended to increase with oilseed rape growth when Se was applied at 0, 1.0, and 2.5 mg kg−1. The ranges of DOC in the two periods were 9.09–12.44 mg L−1 (control), 11.62–13.98 mg L−1 (application of 1 mg kg−1 Se), and 13.12–14.93 mg L−1 (application of 2.5 mg kg−1 Se). When Se was applied at 5.0 and 10.0 mg kg−1, the DOC of the rhizosphere soil solution decreased with the growth of oilseed rape. The ranges of DOC were 11.21–12.15 mg L−1 (5.0 mg kg−1 Se was applied) and 10.38–11.60 mg L−1 (10.0 mg kg−1 Se was applied) in the two periods, respectively.
The specific trends of DOC in the rhizosphere soil solution of each treatment in different periods were as follows: The DOC of the rhizosphere soil solution showed an increasing and then decreasing trend with an increase in exogenous Se application in both periods. In each period, the DOC of the rhizosphere soil solution reached its highest at 2.5 mg kg−1 Se application, which was 13.64 ± 0.45 mg L−1 at 6 weeks and 13.98 ± 0.73 mg L−1 at 8 weeks of seedling emergence, respectively. At 6 weeks after oilseed rape seedling emergence, the DOC of the control treatment was the lowest at 9.96 ± 0.70 mg L−1, whereas, at 8 weeks, the DOC in the 10.0 mg kg−1 Se treatment was the lowest at 11.00 ± 0.50 mg L−1.
No significant difference was observed in the DOC of the non-rhizosphere soil solution for all treatments. At 6 and 8 weeks after oilseed rape seedling emergence, the DOC of the rhizosphere soil solution was higher than that of the non-rhizosphere soil solution by 1.41 and 1.43 times, respectively (Figure 2).

3.2. Effect of Exogenous Se Application on Soil Se Content and Speciation

3.2.1. Soil Total Se

The total Se content in both the rhizosphere and non-rhizosphere soils increased with an increase in exogenous Se concentration and showed significant and positive correlations (p < 0.05) (Table 2). In addition, the total Se content in the non-rhizosphere soils was higher than that in the rhizosphere soils. With the growth of oilseed rape, the total Se content in both the rhizosphere and non-rhizosphere soils decreased.

3.2.2. Se Speciation in Soil

For the rhizosphere soils, the content of three forms of Se increased with an increase in exogenous Se concentration, which showed a significant correlation with the imposed concentration of selenite (p < 0.05) (Table 3). The contents of the three forms of Se in descending order were as follows: organic state > exchangeable state > water-soluble state. Meanwhile, the ratio of the sum of the three forms of Se content to total Se also increased with an increase in exogenous Se concentration, with increases from 24.38% and 20.84% in the control treatment to 54.72% and 53.11% under 10.0 mg/kg applied Se at 6 and 8 weeks after the emergence of rapeseed seedlings, respectively. These findings indicate that the higher the amount of exogenous Se applied, the higher the Se availability in the soil and the more favorable the Se absorption by rapeseed. During the two experimental periods, the content of water-soluble Se in the soil of the control treatment increased slightly with rapeseed growth, whereas the content of water-soluble Se in the other treatments and the content of exchangeable and organic Se in all treatments decreased continuously with rapeseed growth.
For non-rhizosphere soils, the contents of three forms of Se also increased as the exogenous Se concentration increased and showed a significant correlation with the exogenous Se concentration (Table 4). The order of their contents was the same as that of rhizosphere soils, with the content of Se in the organic state being significantly higher than that of Se in the water-soluble and exchangeable states. The content of three forms of Se in all treatments decreased with the growth of oilseed rape.
A comparison of the contents of the three forms of Se in the rhizosphere and non-rhizosphere soils showed that the water-soluble Se content was higher in the rhizosphere soil than in the non-rhizosphere soil under both the control and 1 mg kg−1 Se treatment. Moreover, the water-soluble Se in the non-rhizosphere soil was higher than that in the rhizosphere soil under other Se treatments. The exchangeable Se in the rhizosphere soil (6 weeks: 16.6 µg kg−1, 8 weeks: 14.5 µg kg−1) was higher than that in the non-rhizosphere soil (6 weeks: 15.8 µg kg−1, 8 weeks: 13.8 µg kg−1) under the control treatment. However, the content of exchangeable Se in the non-rhizosphere soil was higher than that in the rhizosphere soil under all other Se application treatments, while the content of organic Se was higher than that in the rhizosphere for all treatments.

3.3. Effect of Exogenous Se Application on Oilseed Rape

3.3.1. Oilseed Rape Biomass

Within the concentration gradient set in this study (Table 5), at 6 weeks after seedling emergence, the root biomass of oilseed rape in all treatments showed a tendency to increase and then decrease with an increase in exogenous Se concentration, and the biomass was the smallest in the 10.0 mg kg−1 of Se treatment. However, the difference between 10.0 mg kg−1 Se treatment and control did not reach a significant level. The highest biomass value was obtained at 2.5 mg kg−1 Se, and it was 1.82 times higher than that of the control treatment. At 8 weeks after seedling emergence, the root biomass of oilseed rape was lower than that of the control at 5.0 and 10.0 mg kg−1 Se but higher than that of the control at other Se application rates. The maximum biomass of oilseed rape roots was found at 2.5 mg kg−1 Se, which increased 48% compared to the control.
Changes in the leaf biomass of oilseed rape with exogenous Se concentrations followed the same trend as that of the root system. At 6 weeks after seedling emergence, the lowest biomass was still observed at 10.0 mg kg−1 Se, although the difference with the control treatment did not reach significance. The highest biomass was observed at 2.5 mg kg−1 Se, which was 1.58 times that of the control. Eight weeks after seedling emergence, the biomass of oilseed rape leaves showed an increasing and then decreasing trend with an increase in exogenous Se concentration, which was the largest at 2.5 mg kg−1 Se, with a significant increase of 32% compared with that of the control treatment. However, the leaf biomass at 10.0 mg kg−1 Se application decreased significantly by 61.02% compared with that of the control.
The trends in the biomass of oilseed rape roots and leaves with exogenous Se concentration at different periods show that the biomass of roots and leaves of oilseed rape reached the highest values at 2.5 mg kg−1 Se, whereas toxic effects appeared at 10.0 mg kg−1 Se for 6 weeks and at 5.0 mg kg−1 Se for 8 weeks, respectively.

3.3.2. Se Content of Oilseed Rape

Figure 3 shows the changes in the Se content of oilseed rape roots and leaves based on the exogenous Se concentrations at different periods. A significant positive correlation was observed between the Se content of oilseed rape roots and leaves and exogenous Se concentration.
Compared with the control, the Se content of oilseed rape at 6 weeks after seedling emergence was 8, 25, 52, and 106 times higher in the root system and 13, 40, 74, and 150 times higher in the leaves than that in the control treatment when 1.0, 2.5, 5.0, and 10.0 mg kg−1 selenite were applied to the soil, respectively. At 8 weeks after seedling emergence of oilseed rape, the Se content of the root system was higher than that of the Se content at 6 weeks for all treatments, while the Se content of the leaves was lower than that of the Se content at 6 weeks. In addition, the Se content of the leaves at 0.0, 1.0, 2.5, 5.0, and 10.0 mg kg−1 of Se application decreased from 0.07 ± 0.01, 0.98 ± 0.12, and 2.92 ± 0.07, 5.38 ± 0.10, and 10.92 ± 0.08 mg kg−1 at 6 weeks to 0.06 ± 0.01, 0.77 ± 0.03, 2.59 ± 0.03, 5.18 ± 0.15, and 9.74 ± 0.20 mg kg−1 at 8 weeks, respectively.

3.3.3. Rape Leaf Bioindicators

(1)
GPx Activity
As shown in Figure 4, the GPx activity of oilseed rape leaves initially increased and then decreased with increasing exogenous Se concentration. In both periods, the highest leaf GPx activity was observed with 5.0 mg kg−1, Se, which was 49.41% and 81.94% higher than that of the control, respectively. At 6 weeks after seedling emergence, the GPx activity of oilseed rape leaves treated with 10.0 mg kg−1 Se was not significantly different from that of the control. At 8 weeks after seedling emergence, the lowest GPx activity of 191 nmol−1 min−1 g−1 was found in the leaves of the control treatment, and significantly higher GPx activities were observed in the leaves of the other treatments compared with the control (p < 0.05). A comparison of the different periods showed that the GPx activity of oilseed rape leaves in all treatments decreased with oilseed rape growth.
(2)
MDA Content
Figure 4 shows that the MDA content in the leaves increased gradually with the growth of oilseed rape and tended to decrease and then increase with an increase in exogenous Se concentration. The lowest levels in both periods were reached at 5.0 mg kg−1 Se, and their MDA contents decreased by 23.18% and 39.25%, respectively, compared with the control. At 6 weeks after seedling emergence, the highest MDA content (54 nmol g−1) was found in leaves under the control treatment, and at 8 weeks after seedling emergence, the MDA content of leaves under the control and 10.0 mg kg−1 Se application increased rapidly along with rapeseed growth by 41.09% and 83.19%, respectively, compared with that at 6 weeks.

4. Discussion

4.1. Effect of Exogenous Se Application on Soil Solution pH and DOC

Researchers have shown that soil Se availability is affected not only by external factors but also by soil properties [20]. Soil pH and organic matter content are considered to be two of the most important chemical factors directly affecting the availability of Se and its effective utilization [30,31]. In this study, the rhizosphere soil solution of oilseed rape was increased by 0.03–0.34 pH units compared to the non-rhizosphere soil solution. The result was in agreement with Luo et al. [32], who found that zinc/cadmium-induced root exudates increased soil solution pH in the rhizosphere of hyperaccumulator Thlaspi caerulescens. Some studies generated the opposite results and showed that significant acidification occurs at the rhizosphere interface to increase the effectiveness of rhizosphere soil nutrients (e.g., zinc, cadmium, iron, phosphorus, and potassium) and stimulate their uptake by plants [33,34,35,36]. Changes in pH variation owing to plants may be related to the charge balance at the soil-root interface. Nye [37] reported that plants could maintain electroneutrality at the root-soil interface by releasing OH or H. Bravin et al. [38] used lime treatment to obtain copper-contaminated soils with different pHs and found that the rhizosphere soil solution of oilseed rape was alkalized when the soil pH was lower than 7.3, whereas the rhizosphere soil solution was acidified when the soil pH was higher than 7.3. In addition, the rhizosphere is a unique system that contains an abundance of microbes, modulating complex biochemical processes. Further studies are needed to consider the effect of rhizosphere microorganisms on the pH of the soil solution.
In the present study, we found that the DOC concentrations in the rhizosphere soil solution of oilseed rape were greater than those in the non-rhizosphere soil solution. This result is in accordance with Oram et al. [39], who reported that the organic matter content in the rhizosphere of aster (Symphyotrichum eatonii) was 1.29–1.84 times higher than that of the non-rhizosphere soils. With the increase in exogenous Se concentration, the rhizosphere soil solution DOC showed a tendency to increase and then decrease, reaching its highest at 2.5 mg kg−1 Se. This phenomenon suggested that moderate Se application (1.0–2.5 mg kg−1) in the soil resulted in greater DOC for the rhizosphere. The reason might be that the suitable Se levels increased soil microbial diversity [13] and enhanced the formation of root exudates by improving plant photosynthesis [40]. Furthermore, more DOC will be formed and released into the rhizosphere soils. The content and composition of DOC in turn affect solubility, bioavailability, toxicity, and the cycling of nutrient and microbial abundance in soils [39].

4.2. Effect of Exogenous Se Application on Soil and Oilseed Rape Se

4.2.1. Soil and Oilseed Rape Se Content

According to the results, exogenous Se application significantly increased the total Se, water-soluble Se, exchangeable Se, and organic Se contents in soils. When 2.5, 5.0, and 10.0 mg kg−1 Se were applied, the soil water-soluble Se, exchangeable Se, and organic Se in the rhizosphere of oilseed rape were lower than those in the non-rhizosphere, which was in accordance with Ma et al. [41]. Munier-Lamy et al. [42] also found that soil soluble and exchangeable Se was lower in rhizosphere soil than in non-rhizosphere soil during the cultivation of maize, lettuce, radish, and ryegrass.
The addition of sodium selenite to the soil significantly increased the concentration of Se in the rapeseed roots and leaves, and most of the Se accumulated in the roots. These findings were consistent with Li et al. [43], who reported that Se(IV) was rapidly converted into organic Se compounds after entering the roots, stored in the root system, and only part of Se(IV) was transported to the leaves through the ligament or xylem. Similar results were observed in rice [44] and maize grain [45] Se concentrations.

4.2.2. Relationship between Soil Se Speciation and Oilseed Rape Se Content

The results of correlation and linear analyses may be biased owing to the covariance of the impact factors on oilseed rape Se content. Therefore, we performed multivariate canonical correlation and ridge regression analyses to explore the relationship between soil Se speciation and oilseed rape Se content [46]. The results showed a significant positive correlation (p < 0.05) between the pairs of canonical correlation variables, with a correlation coefficient of 0.998. The canonical variable “X1” could explain 99.7% of the information for group X (including “x1”, “x2”, and “x3”), while the canonical variable “Y1” explained 99.6% of the information in group Y (including “y1” and “y2”). According to the canonical coefficient matrix results, the linear relationships between the original and canonical variables were as follows:
X1 = 0.004x1 − 1.042x2 − 0.571x3
Y1 = −0.079y1 − 0.088y2
where “x1” represents rhizosphere soil water-soluble Se, “x2” represents rhizosphere soil exchangeable Se, “x3” represents rhizosphere soil organic Se, “y1” represents oilseed rape root Se, and “y2” represents oilseed rape leaf Se. Based on these results, a correlation diagram was plotted, as shown in Figure 5. A significant correlation can be inferred between the Se content of the oilseed rape leaves and root system and the three forms of rhizosphere soil Se based on the good level of linearity.
Based on the results of canonical correlations, ridge regression was used to analyze the Se content of oilseed rape leaves and the influencing factors, including rhizosphere soil solution pH, DOC, and the three forms of rhizosphere soil Se. The regression equation was as follows:
Y = 3.347 − 0.879X1 + 0.078X2 + 0.032X3 + 2.939X4 + 0.964X5
where “X1” represents soil solution pH, “X2” represents soil solution DOC, “X3” represents soil water-soluble Se, “X4” is the soil exchangeable Se, “X5” is the soil organic Se, and “Y” is the Se content of oilseed rape leaves. The results showed a significant regression relationship between the independent and dependent variables, and the model fit was excellent (Table 6). The content of Se in rape leaves could be predicted by this equation.

4.3. Effect of Exogenous Se Application on Oilseed Rape Growth and Physiological Traits

Previous studies revealed that biomass was a good index for evaluating the growth state of plants [47]. In this study, soil Se application of ≤2.5 mg kg−1 level increased the biomass of oilseed rape roots and leaves but decreased when Se level ≥ 5.0 mg kg−1. The results indicated that exogenous Se application showed “low promotion and high inhibition” effects on plant growth. Our results were consistent with the previous studies, which reported that low concentrations of Se could promote plant growth and increase tolerance to abiotic stresses [48,49,50,51], while high concentrations of Se inhibit plant growth [52]. Such findings have been reported in a wide range of plants, including white lupine, sunflower, cabbage, canola, rapeseed, and spinach [51,53,54].
Selenium is necessary as a cofactor for GPx production, which maintains a balance between free radical production and scavenging. This enzyme reduces cellular peroxides and prevents harmful oxidation in cells. By contrast, MDA is a good indicator of oxidative damage. Therefore, the GPx activity and MDA content of oilseed rape leaves under exposure to different Na2SeO3 concentrations were investigated. In the present research, low concentrations of Se (≤5.0 mg kg−1) led to a remarkable rise in GPx activity and a decline in MDA content. In a study by Liu et al. [55], it was found that a small amount of Se (≤10.0 mg kg−1) could enhance root vigor, improve root architecture, and further promote rapeseed growth by increasing the antioxidant enzyme activity and the content of MDA in the root system. In another study, Ulhassan et al. [56] showed that glutathione reductase (GR) activity increased and MDA content decreased in the leaves of four Brassica napus cultivars under 25 μM Se(Ⅳ) compared to that of the control. In addition, other studies have reported that moderate amounts of Se can improve the adaptive ability and antioxidant capacity of plants under abiotic stress environments [57,58,59]. El-Badri et al. [60] reported that Se application (5–150 μmol L−1 Se nanoparticles) significantly increased the activity of ascorbate (AsA) and glutathione (GSH) in rape seedlings, reduced the MDA content, and improved the adaptive capacity of rapeseed under salinity stress conditions. Djanaguiraman et al. [61] demonstrated that, under high temperature stress, Se increased the antioxidant capacity of sorghum, reduced the reactive oxygen species (ROS) and MDA content, and consequently attenuated cell membrane damage. However, excessive Se can also trigger plant selenosis because selenocysteine/selenomethionine can be incorrectly inserted into the protein chain instead of cysteine/methionine, leading to selenoprotein aberrations [62]. In contrast, Se can also act as a pro-oxidant, generating ROS and triggering oxidative stress [63]. These findings suggest that Se has a protective effect on plant cell membranes within a certain concentration range, whereas excessive Se levels can lead to peroxidation and affect plant growth and development.

5. Conclusions

Soil Se application significantly increased the Se concentration in oilseed rape roots and leaves. Canonical correlation and ridge regression analyses revealed that rape Se accumulation relies largely on the content of water-soluble, exchangeable, and organic Se in the rhizosphere soil. Amendment with Se significantly improved the contents of water-soluble, exchangeable, and organic Se in soils. The application of 1.0–2.5 mg kg−1 Se had a prominent positive effect on the growth of oilseed rape, enhanced glutathione peroxidase activity, and decreased malondialdehyde content. The root exudates of oilseed rape further increased the pH and dissolved organic carbon of the rhizosphere soil solution. High rates of Se (5.0 and 10.0 mg kg−1) resulted in a significant decrease in rape biomass at the eighth week. Overall, this study found that Se supplementation at 2.5 mg kg−1 could be an effective method for Se biofortification in oilseed rape. However, this study was conducted in the pot experiment, so the obtained result needs to be further confirmed in the field experiment. Moreover, further studies are needed to elucidate the Se biofortification of oilseed rape from plant growth, as well as the soil physico-chemical properties and microbial community composition.

Author Contributions

Conceptualization, Y.X. and Y.L.; methodology, Y.X. and Y.L.; software, Y.X.; validation, Y.X.; formal analysis, Y.X.; investigation, Y.X.; resources, Y.X. and Y.L.; data curation, Y.X.; writing—original draft preparation, Y.X.; writing—review and editing, Y.X. and Y.L.; visualization, Y.X.; supervision, Y.L.; project administration, Y.X. and Y.L.; funding acquisition, Y.X. and Y.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (No. 41671499), the Science and Technology Innovation Fund of Shanxi Agricultural University (No. 2020BQ65), and the Award for Excellent Doctoral in Shanxi (No. SXYBKY2020012).

Data Availability Statement

The data presented in this study are available on request from the corresponding authors.

Acknowledgments

We give special thanks to Pang Xiaoming from the College of Biological Sciences and Technology, Beijing Forestry University, for his assistance in the experiment.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Changes in pH of the rhizosphere and non-rhizosphere soil solutions during different growth periods of oilseed rape. Different lowercase letters represent significant differences between exogenous Se treatments (p < 0.05).
Figure 1. Changes in pH of the rhizosphere and non-rhizosphere soil solutions during different growth periods of oilseed rape. Different lowercase letters represent significant differences between exogenous Se treatments (p < 0.05).
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Figure 2. Changes of DOC in the rhizosphere and non-rhizosphere soil solutions of rape at different growth periods. Different lowercase letters represent significant differences between exogenous Se treatments (p < 0.05).
Figure 2. Changes of DOC in the rhizosphere and non-rhizosphere soil solutions of rape at different growth periods. Different lowercase letters represent significant differences between exogenous Se treatments (p < 0.05).
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Figure 3. Effect of exogenous Se application on Se content of oilseed rape at different periods. Different lowercase letters represent significant differences between exogenous Se treatments (p < 0.05).
Figure 3. Effect of exogenous Se application on Se content of oilseed rape at different periods. Different lowercase letters represent significant differences between exogenous Se treatments (p < 0.05).
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Figure 4. Effects of exogenous Se application on physiological indices of rape leaves at different stages. Different lowercase letters represent significant differences between exogenous Se treatments (p < 0.05).
Figure 4. Effects of exogenous Se application on physiological indices of rape leaves at different stages. Different lowercase letters represent significant differences between exogenous Se treatments (p < 0.05).
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Figure 5. Relationship and correlation coefficients between canonical variables.
Figure 5. Relationship and correlation coefficients between canonical variables.
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Table 1. Basic physical and chemical properties of the test soil.
Table 1. Basic physical and chemical properties of the test soil.
Clay
(%)
Silt
(%)
Sand
(%)
pHElectrical Conductivity
(μS cm−1)
Organic Carbon
(g kg−1)
Organic Nitrogen
(g kg−1)
Available Se
(mg kg−1)
1045454.9583.013.631.480.02
Table 2. Effects of exogenous Se application on total Se contents in soil (mg kg−1).
Table 2. Effects of exogenous Se application on total Se contents in soil (mg kg−1).
Se Applied6 Weeks8 Weeks
(mg kg−1)Rhizosphere SoilNon-Rhizosphere SoilRhizosphere SoilNon-Rhizosphere Soil
00.21 ± 0.01 e0.23 ± 0.01 e0.21 ± 0.01 e0.22 ± 0.01 e
11.07 ± 0.03 d1.11 ± 0.03 d1.03 ± 0.01 d1.04 ± 0.02 d
2.52.09 ± 0.01 c2.15 ± 0.03 c2.01 ± 0.05 c2.12 ± 0.02 c
54.19 ± 0.01 b4.32 ± 0.05 b4.13 ± 0.03 b4.31 ± 0.03 b
108.71 ± 0.01 a8.79 ± 0.04 a8.69 ± 0.05 a8.78 ± 0.03 a
Different lowercase letters represent significant differences between exogenous Se treatments (p < 0.05).
Table 3. Effects of exogenous Se application on Se speciation in rhizosphere soil.
Table 3. Effects of exogenous Se application on Se speciation in rhizosphere soil.
Sampling TimeSe AppliedWater-Soluble SeExchangeable SeOrganic Matter-Bound Se
(mg kg−1)Content (µg kg−1)Ratio (%)Content (mg kg−1)Ratio (%)Content (mg kg−1)Ratio (%)
6 weeks01.65 ± 0.16 e0.810.02 ± 0.00 e8.090.03 ± 0.00 e15.48
110.65 ± 0.41 d1.000.10 ± 0.01 d9.500.17 ± 0.01 d16.12
2.522.73 ± 3.78 c1.090.25 ± 0.01 c11.920.75 ± 0.01 c35.67
547.37 ± 2.69 b1.130.52 ± 0.01 b12.331.59 ± 0.06 b37.90
10103.57 ± 4.19 a1.191.15 ± 0.03 a13.243.51 ± 0.12 a40.29
8 weeks01.99 ± 0.08 e0.930.01 ± 0.00 e6.760.03 ± 0.00 e13.15
19.65 ± 0.45 d0.940.10 ± 0.00 d9.430.16 ± 0.00 d15.80
2.520.16 ± 0.89 c1.000.24 ± 0.01 c11.740.71 ± 0.03 c35.31
545.27 ± 4.67 b1.100.49 ± 0.03 b11.991.54 ± 0.05 b37.34
1099.62 ± 3.66 a1.151.11 ± 0.04 a12.763.41 ± 0.04 a39.20
Different lowercase letters represent significant differences between exogenous Se treatments (p < 0.05). The ratio is the mass fraction of Se speciation relative to total Se.
Table 4. Effects of exogenous Se application on Se speciation in non-rhizosphere soil.
Table 4. Effects of exogenous Se application on Se speciation in non-rhizosphere soil.
Sampling TimeSe AppliedWater-Soluble SeExchangeable SeOrganic Matter-Bound Se
(mg kg−1)Content (µg kg−1)Ratio (%)Content (mg kg−1)Ratio (%)Content (mg kg−1)Ratio (%)
6 weeks01.63 ± 0.05 e0.700.02 ± 0.00 e6.730.03 ± 0.00 e14.06
19.42 ± 0.41 d0.850.11 ± 0.00 d9.850.18 ± 0.01 d15.88
2.523.23 ± 0.45 c1.080.26 ± 0.02 c12.060.78 ± 0.00 c36.08
551.37 ± 3.43 b1.190.54 ± 0.04 b12.581.60 ± 0.04 b37.05
10112.67 ± 5.23 a1.281.16 ± 0.01 a13.243.62 ± 0.03 a41.11
8 weeks01.48 ± 0.25 e0.680.01 ± 0.00 e6.390.03 ± 0.00 e13.12
18.63 ± 0.27 d0.830.10 ± 0.02 d9.360.16 ± 0.01 d15.65
2.521.36 ± 0.38 c1.010.25 ± 0.02 c11.900.76 ± 0.04 c36.07
548.54 ± 1.86 b1.130.54 ± 0.04 b12.451.58 ± 0.06 b36.77
10107.89 ± 2.85 a1.231.14 ± 0.01 a12.943.61 ± 0.04 a41.10
Different lowercase letters represent significant differences between exogenous Se treatments (p < 0.05). The ratio is the mass fraction of Se speciation relative to total Se.
Table 5. Effects of exogenous Se application on the rape biomass at different stages (g pot−1).
Table 5. Effects of exogenous Se application on the rape biomass at different stages (g pot−1).
Se Applied6 Weeks8 Weeks
(mg kg−1)Root Dry WeightLeaf Dry WeightRoot Dry WeightLeaf Dry Weight
00.06 ± 0.01 b0.24 ± 0.04 c0.09 ± 0.03 b0.31 ± 0.04 b
10.09 ± 0.02 a0.34 ± 0.02 a b0.11 ± 0.01 a b0.36 ± 0.04 b
2.50.11 ± 0.01 a0.38 ± 0.05 a0.13 ± 0.02 a0.41 ± 0.02 a
50.10 ± 0.02 a0.32 ± 0.05 b0.05 ± 0.02 c0.21 ± 0.03 c
100.05 ± 0.01 b0.21 ± 0.01 c0.03 ± 0.01 c0.12 ± 0.03 d
Different lowercase letters represent significant differences between exogenous Se treatments (p < 0.05).
Table 6. Ridge regression analyses of Se content in rape leaves.
Table 6. Ridge regression analyses of Se content in rape leaves.
Parameters in Rhizosphere SoilNon-Standardized CoefficientStandardized CoefficienttpR2Adjustment of R2F
BStandard ErrorBeta
constant3.3473.540-0.9450.3510.9880.986F = 570.495
p = 0.000
Soil solution pH−0.8790.856−0.020−1.0270.312
Soil solution DOC0.0780.0540.0281.4530.155
Soil water-soluble Se0.0320.0010.30735.7580.000 ***
Soil exchangeable Se2.9390.0730.31940.4490.000 ***
Soil organic matter-bound Se0.9640.0260.32737.6020.000 ***
*** represents significance at the 1%.
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Xu, Y.; Li, Y. Effects of Sodium Selenite on the Rhizosphere Environment, Growth, and Physiological Traits of Oilseed Rape (Brassica napus L.). Agronomy 2023, 13, 2508. https://doi.org/10.3390/agronomy13102508

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Xu Y, Li Y. Effects of Sodium Selenite on the Rhizosphere Environment, Growth, and Physiological Traits of Oilseed Rape (Brassica napus L.). Agronomy. 2023; 13(10):2508. https://doi.org/10.3390/agronomy13102508

Chicago/Turabian Style

Xu, Yuefeng, and Yonghua Li. 2023. "Effects of Sodium Selenite on the Rhizosphere Environment, Growth, and Physiological Traits of Oilseed Rape (Brassica napus L.)" Agronomy 13, no. 10: 2508. https://doi.org/10.3390/agronomy13102508

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