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Article

Applied Selenium as a Powerful Antioxidant to Mitigate the Harmful Effects of Salinity Stress in Snap Bean Seedlings

by
Hoda A. S. Farag
1,
Mohamed F. M. Ibrahim
2,
Ahmed Abou El-Yazied
3,
Hossam S. El-Beltagi
4,5,*,
Hany G. Abd El-Gawad
3,
Mohammed Alqurashi
6,
Tarek A. Shalaby
7,8,
Abdallah Tageldein Mansour
9,10,
Abdulmalik A. Alkhateeb
4 and
Reham Farag
2,*
1
Food and Nutrition Science Department, College of Agricultural Science and Food, King Faisal University, Al-Ahsa 31982, Saudi Arabia
2
Department of Agricultural Botany, Faculty of Agriculture, Ain Shams University, Cairo 11566, Egypt
3
Department of Horticulture, Faculty of Agriculture, Ain Shams University, Cairo 11566, Egypt
4
Agricultural Biotechnology Department, College of Agriculture and Food Sciences, King Faisal University, Al-Ahsa 31982, Saudi Arabia
5
Biochemistry Department, Faculty of Agriculture, Cairo University, Giza 12613, Egypt
6
Department of Biotechnology, Faculty of Science, Taif University, Taif 21974, Saudi Arabia
7
Department of Arid Land Agriculture, College of Agricultural and Food Science, King Faisal University, Al-Ahsa 31982, Saudi Arabia
8
Horticulture Department, Faculty of Agriculture, Kafrelsheikh University, Kafr El-Sheikh 33516, Egypt
9
Department of Aquaculture and Animal Production, College of Agriculture and Food Sciences, King Faisal University, Al-Ahsa 31982, Saudi Arabia
10
Department of Fish and Animal Production, Faculty of Agriculture (Saba Basha), Alexandria University, Alexandria 21526, Egypt
*
Authors to whom correspondence should be addressed.
Agronomy 2022, 12(12), 3215; https://doi.org/10.3390/agronomy12123215
Submission received: 1 December 2022 / Revised: 13 December 2022 / Accepted: 15 December 2022 / Published: 18 December 2022
(This article belongs to the Special Issue Antioxidant Defenses in Crop Plants)
Browse Figures
Versions Notes

Abstract

:
Selenium (Se) plays several significant roles in regulating growth, development and plant responses to various abiotic stresses. However, its influence on sulfate transporters (SULTRS) and achieving the harmony with other salt-tolerance features is still limited in the previous literatures. This study elucidated the effect of Se supplementation (5, 10 and 20 µM) on salt-stressed (50 mM NaCl) snap bean seedlings. Generally, the results indicated that Se had dual effects on the salt stressed seedlings according to its concentration. At a low level (5 µM), plants demonstrated a significant improvement in shoot (13.8%) and root (22.8%) fresh weight, chlorophyll a (7.4%), chlorophyll b (14.7%), carotenoids (23.2%), leaf relative water content (RWC; 8.5%), proline (17.2%), total soluble sugars (34.3%), free amino acids (FAA; 18.4%), K (36.7%), Ca (33.4%), K/Na ratio (77.9%), superoxide dismutase (SOD; 18%), ascorbate peroxidase (APX;12.8%) and guaiacol peroxidase (G-POX; 27.1%) compared to the untreated plants. Meanwhile, most of these responses as well as sulfur (S), Se and catalase (CAT) were obviously decreased in parallel with increasing the applied Se up to 20 µM. The molecular study revealed that three membrane sulfate transporters (SULTR1, SULTR2 and SULTR 3) in the root and leaves and salinity responsive genes (SOS1, NHX1 and Osmotin) in leaves displayed different expression patterns under various Se treatments. Conclusively, Se at low doses can be beneficial in mitigating salinity-mediated damage and achieving the functioning homeostasis to tolerance features.

1. Introduction

Climate change represents a serious threat to several agricultural areas worldwide, leading to increased risk of soil salinity and several challenges for sustainable agriculture and food security [1,2]. It has been predicted that 50% of the arable lands in the world will be affected by salinity stress within the next few decades [3]. Accumulation of salts in soil can affect its pore connectivity and hydraulic conductivity [4,5]. These effects lead to difficulties in the growth and productivity of several crops. After exposure to salinity stress, most plant species lose their ability to maximize the rate of photosynthesis [6,7,8]. This response is due to its harmful effect on the photosynthetic pigments [9,10], stomatal conductance [11] and electron transport chain [7]. Furthermore, under saline conditions, plants may be risked by the desiccation due to the osmotic stress [12,13]. Osmotic stress is the direct secondary effect to salinity stress on plants; it occurs due to the decrease in the solute potential of the soil solution leading to hindering of the water uptake by roots [14]. The ionic toxicity is considered the second direct effect of salinity stress on plants due to the hyper-accumulation of toxic ions such as Na+ and Cl− leading to various deleterious effects on cytosolic enzymes and metabolic activities [15,16]. In addition, the cytotoxicity of these ions includes the efflux of cytosolic K+ or Ca2+ leading to the imbalance in their cellular homeostasis [17]. Oxidative stress induced by salinity stress is another main reason to restrict different developmental, physiological, biochemical and molecular aspects in plants [9,10,13]. Salinity stress can cause an excessive release to reactive oxygen species (ROS) leading to several changes in the histochemistry and gene expression and prevents the normal functioning of plants [9,10,13,18]. These changes include the damages to chloroplast structure and function [19]; alternation of the movement of ions across membranes through affecting ion transporters and channel proteins [13,20]; and regulating of osmolytes and antioxidant machinery, including the enzymatic and non-enzymatic antioxidants [9].
Antioxidants supplementation could protect the metabolism and cellular functioning of plants under various abiotic stresses [21,22,23,24,25,26,27]. In this context, selenium (Se) has been found to enhance the antioxidant capacity and protect plants against adverse conditions [28,29]. Selenium (Se) is a vital micronutrient for human health and animals through its significance as anticancer and regulating the metabolism of the thyroid hormone [30,31,32]. As well as this, it plays an important role in the metabolism of microorganisms [33] and in protecting plants against diverse abiotic stresses [34]. In nature, several factors in the soil such as soil texture, pH, organic matter, sulfur content and microbial activity alter the accessibility and allocation of Se [35]. Moreover, the effect of Se on plants depends on its concentration. At low doses, Se can delay senescence, stimulate plant growth, regulate water balance and increase the antioxidant capacity, leading to the protection of plants against a wide array of the stressful factors [17,34,36,37]. Under saline conditions, it prompts photosynthesis, leaf pigments and ion homeostasis and induces progression of downstream signals that help plants to mitigate the accumulation of salts [38]. In addition to its benefits in protecting plants against salt stress, it has been confirmed that Se biofortification can enhance the nutritional value and quality of several crops. In addition, it may compensate its global deficiency in the human diet [39,40]. In contrast, Se at higher concentrations can be toxic (selenosis) due to the ionic radius of Se, and its chemical properties are similar to sulfur (S) [28]. These properties may lead to serious changes in the three-dimensional structure of proteins and the activities of cytosolic enzymes as a result of uptake of Se instead of S and affecting the sulfur-containing amino acids [37,38]. In the soil, Se has been found in different forms such as selenide, elemental Se, selenite or selenate [41]. However, selenate is the most ubiquitous form found in agricultural soils. It is more water-soluble and taken up more readily than selenite [38]. Furthermore, selenate can be absorbed and transported through a wide spectrum of sulfate transporters (SULTRs) and channels in the root cell membranes [42,43]. Recently, SULTRs have been found to play a key role in plant growth, development or abiotic stress responses [43].
Plasma membrane (SOS1) and vacuolar (NHX1) Na+/H+ antiporters are two proteins that are responsible for excluding Na+ ions from the cytosol to outside the plasma membrane or inside the vacuole, respectively [6,10,44]. Osmotin is a cysteine-rich protein synthesized in vacuoles to function as an osmoregulator under low water potential [45]. It can also control the oxidative damage induced by ROS, specifically, H2O2 and isolate Na+, in the vacuoles during salt stress [46]. Furthermore, overexpression of osmotin has been found to reduce lipid peroxidation and increase the proline content under different stresses [47]. These responses enable plants to survive under salt stress by avoiding Na+ toxicity on different plant metabolisms and the maintenance of ion homeostasis in the cytoplasmic matrix.
Snap bean (Phaseolus vulgaris L.) is considered the most consumed legume crop worldwide [48]. It possess high content of phyto-protein, vitamins, micronutrients and fibers [49,50]. Moreover, using it as a primary food source can reduce the risk for many types of cancers [51,52]. As a glycophyte, the snap bean is considered a salt-sensitive crop with a threshold salinity level of 1 dS m−1 [53]. Therefore, enhancing its tolerance to salinity stress has become one of the most important tasks for plant scientists around the world.
Despite the well-known benefits of Se as a powerful antioxidant in mitigating the damage caused by abiotic stresses in several plant species, there are no data in the literature regarding the role of Se in regulating the uptake of sulfate and excluding Na+ ions in the salt-stressed snap bean seedlings. This study tried to explore the role of Se in enhancing plant growth, photosynthetic pigments, accumulation of osmolytes and modulating the activities of antioxidant enzymes in snap bean seedlings under saline conditions. Moreover, it can be hypothesized that applied Se at optimum concentration improved the tolerance of salt-stressed snap bean seedlings by affecting the function of several membrane sulfate transporters (SULTR1, SULTR2 and SULTR3) and a number of salt stress responsive genes (SOS1, NHX1 and Osmotin).

2. Materials and Methods

2.1. Plant Material, Growth Conditions and Treatments

Snap bean (Phaseolus vulgaris L.) seeds (Colter HMX 2117 cv. Clause Company; Medchal; Telangana; India) were sterilized with 0.5% NaOCl (w/v) for 4 min and washed with distilled water 5 times. Seeds were sown in black plastic pots (13 cm diameter & 700 cm3 volume) with an equal quantity of pre-washed sand. Each pot containing three seeds was thinned to one homogenous seedling in size and form after the full germination and seedling growth for 10 days. During this period, each pot was irrigated with 250 mL of ½ strength Hoagland’s solution every 2 days [54]. Starting from the twelfth day, pots were supplemented every 2 days with (a) ½ strength Hoagland’s solution (control), (b) ½ strength Hoagland’s solution + 5 µM Se, (c) ½ strength Hoagland’s solution + 10 µM Se, (d) ½ strength Hoagland’s solution + 20 µM Se, (e) ½ strength Hoagland’s solution modified by adding 50 mM NaCl, (f) ½ strength Hoagland’s solution modified by adding 50 mM NaCl + 5 µM Se, (g) ½ strength Hoagland’s solution modified by adding 50 mM NaCl + 10 µM Se and (h) ½ strength Hoagland’s solution modified by adding 50 mM NaCl + 20 µM Se for an additional 2 weeks. Selenium (Se) was added as sodium selenate (Na2SeO4) which is considered the most ubiquitous form found in the agricultural soils [38]. All pots were kept under greenhouse conditions (Faculty of Agriculture, Ain Shams University, Cairo, Egypt; Latitude: 30.113636 and longitude: 31.2470226). The average air temperature (24.3 ± 5.3) and relative humidity (73.4 ± 2.6) were recorded using a digital Thermo/hygrometer Art placed in the middle of greenhouse (No. 30.5000/30.5002, TFA, Wertheim, Baden-Württemberg, Germany). The experimental layout was complete randomized design (CRD) with three replicates. Twenty-eight old seedlings were collected to determine the various traits. The total number of pots was 192, which equaled 8 treatments × 8 pots × 3 replicates.

2.2. Determination of Growth Parameters and Leaf Pigments

At 28 days after sowing, seedlings were collected to determine the different traits. The root and shoot fresh weights were recorded immediately using a digital balance. Meanwhile, dry weight was determined according to Alsamadany, Mansour, Elkelish and Ibrahim [9]. Chlorophyll a, b and total chlorophyll were determined in the acetone extract using two specific wavelengths at 645 and 662 nm as described by Costache et al. [55]. Carotenoids were quantified using the acetone or petroleum ether method as described by de Carvalho et al. [56] utilizing the following formula: Carotenoids (mg/g FW) = A450 × V (mL) × 10/(A1%1cm × W (g)), where A450 = Absorbance at 450 nm, V = Total extract volume, W = sample weight, A1%1cm = 2592 (β-carotene coefficient in petroleum ether).

2.3. Quantification of Relative Water Content and Osmolytes

Relative water content (RWC) was estimated according to Abd Elbar et al. [57]. The fresh leaf sample (0.2 g) was incubated in 50 mL of distilled water for 4 h. Then, turgid weights of leaf samples were measured. Leaf samples were oven dried to calculate dry weight at 70 °C for 48 h. The RWC was determined by the following equation:
RWC   ( % ) = FW − DW TW − DW × 100
Proline was determined according to the method of Bates et al. [58] with some modifications. Fresh leaves (0.5 g) were ground and homogenized with 4 mL of 100 mM potassium phosphate buffer (pH 6.0). The samples were centrifuged for 10 min at 10,000 rpm. The reaction mixture contained 200 µL of ortho-phosphoric acid, acetic acid and water (15:60:25; V.V.V.). The reaction proceeded for 1 h in a boiling water bath and the developed red dye was extracted with 1 mL of toluene and measured by spectrophotometer at 515 nm. Total soluble sugars were extracted by homogenizing a known weight (0.5 g) of leaves in 10 mL of 80% ethanol for at least 24 h at 0 °C; the alcoholic extract was collected and the remained tissue re-extracted using 10 mL 80% twice. Finally, the collected extract was completed to 50 mL using 80% ethanol. Soluble sugars were estimated according to Chow and Landhäusser [59], which can be summarized as follows: 0.5 mL of extracted solution was mixed with 1 mL of 2% phenol solution followed by rapid addition of 2.5 mL of concentrated sulfuric acid (H2SO4). After 10 min of yellow color development in the dark and an additional 30 min of cooling in a water bath at 22 °C, absorbance was measured at wavelength 490 nm. Free amino acids (FAA) were determined by ninhydrin reagent by reading the developed bluish purple color at 570 nm as glycine according to the method of Yemm et al. [60].

2.4. Measurements of Lipid Peroxidation and H2O2

For evaluating the level of malondialdehyde (MDA), leaf samples (0.1 g) were boiled with 50 mM phosphate buffer. After cooling and centrifuging, 0.5% thiobarbituric acid was added to supernatant and the mixture was homogenized before being analyzed colorimetrically at 532 and 600 nm [61]. The concentration of the MDA/TBA complex was calculated using the following equation:
MDA (nmol·g−1 FW) = (A535 − A600)/ε
where ε is the extinction coefficient = 155 mM−1 cm−1.
Concentration of H2O2 was extracted with 5% (w/v) trichloroacetic acid and determined based on the absorbance change at 415 nm [62].

2.5. Determination of Antioxidant Enzyme Activities

Crude enzyme was extracted by homogenizing 0.2 g of fresh leaf sample in 50 mM potassium phosphate buffer (pH 7.0) containing 0.1 mM EDTA and 1% polyvinylpyrrolidone (w/v). Superoxide dismutase (SOD) assay was based on the method described by Beyer and Fridovich [63]. Reaction mixture with a total volume of 3 mL contained 100 μL crude enzyme, 50 mM phosphate buffer (pH 7.8), 75 μM NBT, 13 mM L-methionine, 0.1 mM EDTA and 0.5 mM riboflavin. The reaction was initiated by addition of riboflavin, then the reaction mixture was illuminated for 20 min with a 20 W fluorescent lamp. One unit of enzyme activity was defined as the amount of enzyme required to result in a 50% inhibition in the rate of nitro blue tetrazolium (NBT) reduction at 560 nm. The activity of ascorbate peroxidase (APX) was determined in the supernatant by mixing 500 mM potassium phosphate buffer, pH 6.0, 0.8 mM ascorbic acid, 1.0 mM hydrogen peroxide. The APX activity was determined by monitoring the ascorbate oxidation rate at 290 nm every 15 s for 3 min, as described by Nakano and Asada [64]. The molar extinction coefficient used was 2.8 mM−1 cm−1. Guaiacol peroxidase (G-POX) activity was determined at 25 °C according to Dias and Costa [65] with some modifications. The reaction mixture contained 2.25 mM guaiacol, 11 mM H2O2 in 0.1 M phosphate buffer (pH 6.0) and 100 mL of enzyme extract in a total volume of 2 mL. G-POX activity was determined by following the increase in absorbance of guaiacol at 470 nm. Catalase (CAT) activity was measured by observing the rate of H2O2 decomposition through monitoring the decrease in absorbance at 240 nm [66]. The enzyme assay mixture contained 18 mM H2O2 in 0.1 M phosphate buffer (pH 7.0) or 100 µL of enzyme extract in a total volume of 2 mL.

2.6. Quantification of Minerals Content

Total Na, K, Ca, S and Se were determined using an atomic absorption spectrometer (AAS-Hitachi, Tokyo, Japan). A measure of 10 g of samples were crushed and weighed in crucible porcelain. The samples were then dried for 5 h in an oven, charred on a hot plate, then ashed for 3 h at an initial temperature of 100 °C automatically rising to a final temperature of 500 °C. Destruction results were allowed to cooled in the desiccator, a few drops of demineralized water spilled through the wall of the crucible porcelain until wet; they were dissolved in 5 mL of nitric acid 5 N, put in a 100-mL volumetric flask, rinsed in crucible porcelain 3 times, each time flushing with 10 mL demineralized water, put in the same volumetric flask, diluted with demineralized water until the marking line, and shaken until homogeneous. The mixture was filtered with filter paper, the first 10 mL of filtrate discarded, the subsequently filtrate accommodated in amber glass bottles, stored, and used for quantitative analysis [67,68,69]. All the standard and sample solutions of Na, K, Ca, S and Se were further measured by atomic absorption spectrometer using sodium, potassium, calcium, Selenium and a sulfur hollow cathode lamp at a wavelength, respectively, of 589.0 nm, 766.5 nm, 422.7 nm, 196.0 nm and 180.7 nm using air acetylene flame; and the measurement results had to be within the concentration range of the series solution of standard sodium, potassium, calcium, selenium and sulfur.

2.7. Genes Relative Expression by qRT-PCR

The primer sequences that were used in this study are listed in Table 1. RNA was extracted using an RNA extraction kit (Sigma-Aldrich, St. Louis, MO, USA). After the reverse transcription of RNA and cDNA, the concentration was adjusted using a NanoDrop™ 2000/2000c spectrophotometer according to manufacturer’s protocol (Promega, Walldorf, Germany). For each assay, 20 μL of total volume with gene specific primers were used, with 4 μL SYBR® Green, 1 μL reverse or 1 μL forward primers, 1 μL cDNA sample and 13 μL nuclease-free water added into each well. The analysis was performed on a Rotor-Gene 6000 (Hilden, Germany). Briefly, the protocol included 95 °C for 12 min, 45 cycles of 95 °C for 15 s, 60 °C for 30 s and 72 °C for 30 s, and the melt curve was held in 0.5 °C increments from 60 °C to 95 °C. The results (3 replicates) were normalized according to the glyceraldehyde-3-phosphate dehydrogenase (GAPDH) housekeeping gene, and relative gene expression was presented according to the 2∆DDCt method [65].

2.8. Statistical Analysis and Figures Preparation

The statistical analysis was conducted utilizing Duncan’s Multiple Comparison test (One-way ANOVA) using SAS software 9.1 for windows; p = 0.05 [70]. All measurements were presented as means ± standard error (SE). All figures were prepared using Microsoft Excel 2010.

3. Results

3.1. Effect of Applied-Se on Vegetative Growth

Snap bean seedlings exposed to salinity stress demonstrated an obvious and significant decrease in the biomass accumulation compared to the unstressed conditions (Figure 1). This reduction included the fresh and dry weights for the shoot and root systems compared to those of non-saline conditions. Applied Se displayed varying results according to its concentration. Generally, the growth parameters of seedlings treated with 5 µM Se were improved significantly compared to the untreated plants either under non-saline or saline conditions. In this context, the highest significant results in shoot fresh weight (13.8%), shoot dry weight (35.4%), root fresh weigh (22.8%) and root dry weight (7.5%) were obtained by the treatment of 5 µM Se compared to the untreated plants under saline conditions. In contrast, all examined growth parameters were progressively inhibited with increasing the concentration of applied Se up to 20 µM.

3.2. Effect of Applied-Se on Leaf Pigments

A similar trend to growth was observed in the content of photosynthetic pigments including Chl a, Chl b, Chl a + b or carotenoids (Figure 2), since applied Se displayed dual effects on the photosynthetic pigments according to its concentration. Plants treated with 5 µM Se exhibited a significant increase in Chl a (7.4%), Chl b (14.7 %), Chl a + b (9.6 %) and carotenoids (23.2%) compared to the untreated plants under saline conditions. However, the treatments of Se at 10 and 20 µM obviously reduced all these attributes. Generally, the lowest significant findings were achieved by Se at 20 µM under saline conditions.

3.3. Effect of Applied Se on RWC and Osmolytes

Under saline conditions, all Se-treated and non-treated plants exhibited a significant decrease in RWC compared to the unstressed plants (Figure 3A). Meanwhile, no significant changes were observed under non-saline conditions. The results indicated that applied Se at 5 or 10 µM significantly enhanced RWC by 8.5 and 3.2%, respectively, compared to the untreated plants under saline conditions. In contrast, the treatment of 20 µM Se significantly reduced RWC compared to the untreated plants. On the other hand, there was a significant accumulation in proline, total soluble sugars and free amino acids in salt-stressed plants compared to those of unstressed conditions (Figure 3B–D). The highest significant results in proline (17.2%) and total soluble sugars (34.3%) were obtained by the treatment of 5 µM Se compared to the untreated plants under saline conditions. However, the maximum accumulation of free amino acids (47.2%) was achieved by the treatment of 20 µM Se under saline conditions. Under non-saline conditions, all Se treatments exhibited a significant improvement in total soluble sugars and free amino acids compared to the untreated plants, but proline was enhanced by the treatment of Se at 5 µM.

3.4. Effect of Applied-Se on the Accumulation of MDA and H2O2

Salt-stressed plants demonstrated higher oxidative stress as a result to increase the rate of lipid peroxidation (MDA) and accumulation of H2O2 (Figure 4). Plants treated with 5 µM Se showed a significant decrease in MDA (22.8%) and H2O2 (24.2%) compared to the untreated plants under saline conditions. A similar trend was observed in H2O2 by Se at 10 µM. Meanwhile, Se at 20 µM aggravated the oxidative damage by increasing the accumulation of MDA (25.4%) and H2O2 (17.8%) over the untreated plants under saline conditions. On the other hand, no significant changes were observed in MDA and H2O2 under non-saline conditions.

3.5. Effect of Applied Se on the Activities of Antioxidant Enzymes

Under saline conditions, snap bean seedlings demonstrated a significant increase in the activities of antioxidant enzymes including SOD, CAT, G-POX and APX compared to those grown under non-saline conditions (Figure 5). Plants treated with 5 µM Se showed a significant and greater activity in SOD (18.1%), APX (12.8%) and G-POX (27.1%) compared to the untreated plants under saline conditions. However, plants treated with 5 µM Se showed a significant decrease in CAT by 14.1% compared to the untreated plants under saline conditions. Conversely, increasing the dose of applied Se to 20 µM negatively affected all investigated antioxidant enzymes.

3.6. Effect of Applied Se on the Mineral Contents

Snap bean seedlings exposed to salinity stress demonstrated several changes in K, Na, Ca, K/Na ratio, S and Se compared to those grown under non-saline conditions (Figure 6). It was observed that salinity stress without Se treatments negatively and significantly affected K, Ca, K/Na ratio and S compared to the unstressed conditions. However, Na exhibited greater accumulation in the salt-stressed plants but no changes in Se. On the other hand, plants treated with 5 µM Se showed an improvement in K (36.7%; 7.8%), Ca (33.4%; 21.7%), K/Na ratio (77.9%; 17.6%) and Se (952%; 175.6%) compared to the untreated plants in both saline and non-saline conditions, respectively. Conversely, applied Se at 5 µM significantly decreased Na (23.3%) and S (20.3%) compared to untreated plants under saline conditions. This decrease was aggravated with increasing concentration of applied Se up to 20 µM.

3.7. Effect of Applied Se on the Expression of Sulfate Transporter (SULTRs) Genes

Three sulfate (SO42−) transporter genes including SULTR1, SULTR2 and SULTR3 were investigated for their expression patterns in snap bean seedlings under saline and non-saline conditions (Figure 7). It was observed that SULTR1 in the root was significantly downregulated compared to the untreated plants under saline and non-saline conditions. This response was more obvious by the treatments of Se at 10 and 20 µM relative to 5 µM. A similar trend was observed in the expression of root SULTR2 and SULTR3 under non-saline and saline conditions, respectively. On the other hand, SULTR2 in roots did not reveal any significant changes under saline conditions. Meanwhile, SULTR3 in the root was dramatically declined by Se at 20 µM. Similarly, the relative expression of SULTR2 and SULTR3 in leaves was significantly downregulated with increasing the concentration of Se applications either under saline or non-saline conditions. As for SULTR1 in leaves, it showed a significant up-regulation with the treatment of Se at 5 µM under saline conditions, while it followed a similar pattern to SULTR2 and SULTR3 under non-saline conditions.

3.8. Effect of Applied Se on the Salt Stress Responsive Genes

Snap bean seedlings treated with various Se applications under saline or non-saline conditions displayed different patterns of expression to the plasma membrane Na+/H+ antiporter protein (SOS1), vacuolar Na+/H+ antiporter protein (NHX1) and Osmotin as a defensive protein against a wide array of biotic and abiotic stresses (Figure 8). The results indicated that the expression of SOS1, NHX1 and Osmotin was significantly upregulated under saline stress compared to the unstressed conditions. The highest upregulation in NHX1 and Osmotin under saline conditions was achieved by the treatment of Se at 5 µM compared to the other treatments. However, the highest significant upregulation in SOS1 was shown by Se at 20 µM under saline conditions. These findings imply that NHX1 and Osmotin were downregulated in parallel with an increase of the concentration of Se under saline conditions, but SOS1 was upregulated under the same conditions. On the other hand, no changes in SOS1, NHX1 were detected between different Se-treated and non-treated plants under non-saline conditions. Meanwhile, Osmotin was obviously and significantly upregulated with applied Se at 5 µM under non-saline conditions.

4. Discussion

Salinity stress is considered one of the most adverse environmental factors that can restrict plant growth or development. This effect could be attributed as hindering the rate of cell division, elongation and cytogenetic activities [71,72,73]. Furthermore, the toxic effect of salts ions (Na+ & Cl−) can negatively affect photosynthesis [6], phytohormones [74], the balance of plant water status [75] and nutrients homeostasis [76,77]. In this study, applied Se at 5 µM exhibited the highest significant improvement in growth parameters compared to the other treatments under non-saline and saline conditions, whereas raising Se concentration up to 20 µM showed an obvious and significant decrease. Several lines of evidence proved that Se in plants has a narrow range between essentiality and toxicity [17,37,38]. At low doses, it can enhance plant growth through promoting the efficiency of photosynthesis and enhancing the chloroplast antioxidant defense system [38]. Many previous studies have found that applied Se at optimal levels can stimulate plant growth and confer salt tolerance in many plant species, i.e., canola [78], tomato [79] lettuce [80], maize [36] and wheat [17]. Conversely, the high levels of Se can cause a significant inhibition to plant growth and various biochemical attributes like photosynthesis and ion homeostasis. In this respect, it has been found that exogenous Se at 100 µM severely inhibited the growth parameters of potato plants under drought stress compared to 10 µM which demonstrated a protective role and achieved many benefits to plants under such conditions [37]. Moreover, the treatment of Se at 5 µM was more effective in enhancing wheat tolerance to salinity stress compared with 10 µM [17]. Meanwhile, applied Se at 40 µM strongly inhibited the growth of the root system in Arabidopsis thaliana L [81].
In this study, photosynthetic pigments including Chl a, Chl b, Chl a + b and carotenoids followed the similar trend of growth parameters. Under saline conditions, applied Se at low concentrations has been found to enhance the leaf content of photosynthetic pigments in many plant species [17,79,82,83]. For instance, 1 µM Se significantly improved the chlorophyll content of salt-stressed maize seedlings, but 25 µM Se showed an inhibitory effect on chlorophyll [83]. Furthermore, applied 5 µM Se was more effective in enhancing the chlorophyll and carotenoids of salt-stressed wheat seedlings than 10 µM Se [17]. This improvement could be attributed to the ability of Se at low doses to reduce the damage of chloroplast and maintain its ultrastructure under salinity stress [83], since most photosynthetic pigments are synthesized and localized in the chloroplast membranes [84].
Under saline conditions, plants accumulate a high concentration of low molecular-mass organic solutes such as proline, soluble sugars and free amino acids to regulate the osmotic potential of cells aiming at improving water absorption under such conditions [6,10,13,22]. In this study, applied Se specifically at 5 µM improved RWC, while Se at 20 µM reduced this response under saline conditions. Se supplementation at an optimal level can regulate the plant water status under desiccation induced by salinity [17] and drought stress [37]. These effects could be attributed to the ability of Se at low concentrations to protect the integrity of cell membranes from the salt stress-induced oxidative damage [38,82]. In contrast, Se at high levels could cause a replacement to sulfur ions with selenium leading to severe changes to protein which contributes to cell membranes structure and functioning [29,38]. As for the positive effect of applied Se at 5 µM on proline, this effect could be attributed to the ability of Se to increase the activity of γ-glutamyl kinase and reduce the activity of proline oxidase leading to an increase in proline biosynthesis and a reduction of its degradation [17,85]. In addition, enhancing the content of soluble sugars by Se at 5 µM under saline conditions could be related to the improvement of photosynthesis and maintaining RWC. On the other hand, increasing free amino acids by Se at 20 µM may be attributed to the inhibition of protein synthesis or stimulation of its degradation under saline conditions.
It has been documented that salt stress can induce oxidative damage to plant tissues as a result of the excessive production of reactive oxygen species [6,9,10,13]. These molecules at high levels can impair plant cell components from nucleic acids, proteins and lipids, and at severe levels may lead to cell death [83,86]. In this context, salinity stress was reported to mediate a decline in plant cell membrane stability due to increasing the activity of lipoxygenase activity and consequently reducing the rate of polyunsaturated fatty acids [87,88]. In this study, the plant exposed to salt stress revealed a significant increase in the rate of lipid peroxidation (MDA) and H2O2 compared to the non-saline conditions. Plants treated with Se at 5 µM exhibited an obvious decrease in MDA and H2O2, while the treatment of Se at 20 µM aggravated the oxidative damage induced by salinity stress. These results may imply the protective or harmful effects of Se on salt-stressed snap bean seedlings according to its applied concentration.
Applied Se can be involved in plant tolerance to salt stress by affecting the activities of several antioxidant enzymes. In this context, it has been confirmed that Se is involved in the formation of glutathione peroxidase (GPx) [89]. Furthermore, several lines of evidence indicated that applied Se at a low concentration can enhance the activities of antioxidant enzymes such as SOD, APX, CAT, G-POX, GR and GST under salinity stress [17,36,79,83]. In this study, plants treated with 5 µM Se exhibited higher activities in SOD, APX and G-POX compared to the untreated plants. However, an opposite trend was observed in CAT with an increase of the concentration of applied Se. SOD is considered the first defensive line against salt-induced oxidative damage by converting the produced superoxide radicals to H2O2 [90]. After that, it is important to eliminate the hyperaccumulation of H2O2 using another enzymatic mechanism [12,21,57,91]. Here, G-POX, CAT and APX play a key role in reducing the generated H2O2 by different pathways. This integration between different antioxidant enzymes was observed between SOD, APX and G-POX under the circumstances of this study. However, the opposite trend of CAT may imply that CAT might be sensitive to the concentration of applied Se in the salt-stressed snap bean seedlings.
In this study, applied Se at low concentration (5 µM) was found to improve the leaf content of K, Ca, K/Na ratio and Se either under saline or non-saline conditions. In contrast, Na was markedly decreased in Se-treated plants at 5 µM, in particular, under saline conditions. Applied Se at the optimum concentration can increase the activities of tonoplast proteins like H+ ATPase and Na+/H+ antiporters in the roots leading to preventing the uptake of Na+ and increasing the K/Na ratio [92]. These responses could maintain the osmotic balance and protect the different vital processes in Se-treated plants under saline conditions [93]. On the other hand, S was dramatically decreased in parallel with increasing the concentration of applied Se either under saline or non-saline conditions. The ionic radius of Se is approximately similar to S and has the same chemical properties [28]. Therefore, in the presence of Se, several sulfate transporters (SULTRs) can be involved in the absorption and transporting of Se instead of S [42,43].
Not much is known in the previous literature about the role of Se in regulating the function of sulfate transporters (SULTRs) in snap bean plants under saline conditions. In this study, the relative expression of three sulfate transporter genes (SULTR1, SULTR2 and SULTR3) using qRT-PCR were investigated in the roots and leaves of snap bean seedlings grown under saline and non-saline conditions. The results indicated that there were different expression patterns for all investigated SULTRs between the root and leaf tissues. Although SULTR1, SULTR2 were down-regulated in the roots with applied-Se at 5 µM under non-saline conditions, SULTR3 was not affected under the same conditions. This response was followed by a relative stability in the expression of all studied SULTRs genes between the non-treated and Se-treated plants at 5 µM in the leaves, leading to achieving S homeostasis under non-saline conditions (Figure 6E). In contrast, all examined SULTRs showed an obvious decline in their expression under saline conditions, leading to a decrease in the uptake of sulfate and consequently, a reduction in the concentration of S with an increase in the applied doses of Se (Figure 6E). In addition, it was obvious that the distinct inhibition of SULTR2 in roots under salinity stress may be attributed to NaCl stress and not to Se applications (Figure 7B).
Besides SULTRs genes, the salt-stress responsive genes, including salt overly sensitive gene (SOS1), vacuolar-localized Na+/H+ antiporter protein (NHX1) and the multifunctional osmotic protective protein (Osmotin), were studied (Figure 8). The results indicated that under saline conditions, there is an overexpression in all studied genes compared to plants grown under non-saline conditions. This response enables plants to maintain their osmotic balance and greater K+/Na+ ratio leading to an improvement in their tolerance to salt stress [6,94]. On the other hand, there was an overexpression in SOS1 followed by the decline of NHX1 with Se at 20 µM under saline conditions (Figure 8A,B). This response could refer to an increase in the toxicity of Na+ in the cytosol and a decrease in its transport to the vacuole with a raise in the concentration of applied Se. Conversely, the improvement in the expression of NHX1 and Osmotin with the treatment of 5 µM could explain the protective effect of this optimal concentration in enhancing the growth, osmotic status and tolerance to salinity stress under the circumstances of this study.

5. Conclusions

The present study provided the first evidence that elucidates the importance of applied Se at a low concentration in activating sulfate transporters (SULTRS) and achieving several beneficial roles that can help snap bean plants to mitigate the deleterious effects of salinity stress. Applied Se at a low concentration (5 µM) improved growth, photosynthetic pigments, osmolytes and nutrients’ homeostasis and antioxidant enzymes. Moreover, it regulated the balance between the uptake of Se and S as sulfate through mediating the function of SULTRS, alternation the expression of Na+/H+ antiporters (SOS1 and NHX1) and up-regulation of Osmotin, leading to enhanced plant tolerance under salinity stress. Generally, the different possible protective effects of Se on the salt-stressed snap bean plants can be summarized as shown in Figure 9. Further molecular studies are required in the future to explore the role of Se in regulating different membrane transporter systems and its influences on plant tolerance to salinity stress.

Author Contributions

Conceptualization, H.S.E.-B., M.F.M.I., A.A.E.-Y. and R.F.; methodology, M.F.M.I., H.G.A.E.-G., H.A.S.F., A.A.A. and R.F.; software, A.A.E.-Y. and M.A.; validation, H.S.E.-B., H.G.A.E.-G. and M.A.; T.A.S., A.A.A. and A.T.M.; formal analysis, M.F.M.I., H.A.S.F. and A.T.M.; investigation, H.S.E.-B., M.F.M.I., A.T.M. and R.F.; resources, M.A., H.A.S.F., M.A., T.A.S., A.A.A. and A.T.M.; data curation, H.S.E.-B., H.A.S.F., T.A.S., A.A.A. and A.T.M.; writing—original draft preparation, R.F., A.A.E.-Y. and H.G.A.E.-G.; writing—review and editing, H.S.E.-B., M.F.M.I., M.A., H.A.S.F., T.A.S., A.A.A. and A.T.M.; visualization, A.A.E.-Y. and M.A.; supervision, H.S.E.-B. and H.A.S.F.; project administration, H.S.E.-B. and H.A.S.F.; funding acquisition, H.S.E.-B., H.A.S.F., M.A., T.A.S., A.A.A. and A.T.M. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported through the annual funding track by the Deanship of Scientific Research, Vice Presidency for Graduate Studies and Scientific Research, King Faisal University, Saudi Arabia (Grant No. 1823).

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors thank the Deanship of Scientific Research, Vice Presidency for Graduate Studies and Scientific Research, King Faisal University, Saudi Arabia, for financial support to conduct and publish this research.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 12 03215 g001 550
Figure 1. Effect of Se supplementation at 5, 10 and 20 µM on growth performance (A), shoot fresh weight (B), shoot fresh weight (C), shoot dry weight (D) and root dry weight (E) of non-stressed and salt-stressed (50 mM NaCl) snap bean seedlings (28 days after sowing). The results are expressed as mean values of three measurements ± SE using Duncan’s multiple range test (p = 0.05). Different letters indicate significant differences among the treatments.
Figure 1. Effect of Se supplementation at 5, 10 and 20 µM on growth performance (A), shoot fresh weight (B), shoot fresh weight (C), shoot dry weight (D) and root dry weight (E) of non-stressed and salt-stressed (50 mM NaCl) snap bean seedlings (28 days after sowing). The results are expressed as mean values of three measurements ± SE using Duncan’s multiple range test (p = 0.05). Different letters indicate significant differences among the treatments.
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Figure 2. Effect of Se supplementation at 5, 10 and 20 µM on chlorophyll a (A), chlorophyll b (B), total chlorophyll (C) and carotenoids (D) of non-stressed and salt-stressed (50 mM NaCl) snap bean seedlings (28 days after sowing). The results are expressed as mean values of three measurements ± SE using Duncan’s multiple range test (p = 0.05). Different letters indicate significant differences among the treatments.
Figure 2. Effect of Se supplementation at 5, 10 and 20 µM on chlorophyll a (A), chlorophyll b (B), total chlorophyll (C) and carotenoids (D) of non-stressed and salt-stressed (50 mM NaCl) snap bean seedlings (28 days after sowing). The results are expressed as mean values of three measurements ± SE using Duncan’s multiple range test (p = 0.05). Different letters indicate significant differences among the treatments.
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Figure 3. Effect of Se supplementation at 5, 10 and 20 µM on relative water content; RWC (A), proline (B), total soluble sugars (C) or free amino acids; FAA (D) of non-stressed and salt-stressed (50 mM NaCl) snap bean seedlings (28 days after sowing). The results are expressed as mean values of three measurements ± SE using Duncan’s multiple range test (p = 0.05). Different letters indicate significant differences among the treatments.
Figure 3. Effect of Se supplementation at 5, 10 and 20 µM on relative water content; RWC (A), proline (B), total soluble sugars (C) or free amino acids; FAA (D) of non-stressed and salt-stressed (50 mM NaCl) snap bean seedlings (28 days after sowing). The results are expressed as mean values of three measurements ± SE using Duncan’s multiple range test (p = 0.05). Different letters indicate significant differences among the treatments.
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Figure 4. Effect of Se supplementation at 5, 10 and 20 µM on relative water content; malondialdehyde; MDA (A) and hydrogen peroxide; H2O2 (B) in the leaves of non-stressed and salt-stressed (50 mM NaCl) snap bean seedlings (28 days after sowing). The results are expressed as mean values of three measurements ± SE using Duncan’s multiple range test (p = 0.05). Different letters indicate significant differences among the treatments.
Figure 4. Effect of Se supplementation at 5, 10 and 20 µM on relative water content; malondialdehyde; MDA (A) and hydrogen peroxide; H2O2 (B) in the leaves of non-stressed and salt-stressed (50 mM NaCl) snap bean seedlings (28 days after sowing). The results are expressed as mean values of three measurements ± SE using Duncan’s multiple range test (p = 0.05). Different letters indicate significant differences among the treatments.
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Figure 5. Effect of Se supplementation at 5, 10 and 20 µM on the activity of superoxide dismutase; SOD (A), ascorbate peroxidase; APX (B), guiacol peroxidase; G-POx (C) and catalase; CAT (D) of non-stressed and salt-stressed (50 mM NaCl) snap bean seedlings (28 days after sowing). The results are expressed as mean values of three measurements ± SE using Duncan’s multiple range test (p = 0.05). Different letters indicate significant differences among the treatments.
Figure 5. Effect of Se supplementation at 5, 10 and 20 µM on the activity of superoxide dismutase; SOD (A), ascorbate peroxidase; APX (B), guiacol peroxidase; G-POx (C) and catalase; CAT (D) of non-stressed and salt-stressed (50 mM NaCl) snap bean seedlings (28 days after sowing). The results are expressed as mean values of three measurements ± SE using Duncan’s multiple range test (p = 0.05). Different letters indicate significant differences among the treatments.
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Figure 6. Effect of Se supplementation at 5, 10 and 20 µM on the leaf content of K (A), Na (B), Ca (C), K/Na ratio (D), S (E) and Se (F) of non-stressed and salt-stressed (50 mM NaCl) snap bean seedlings (28 days after sowing). The results are expressed as mean values of three measurements ± SE using Duncan’s multiple range test (p = 0.05). Different letters indicate significant differences among the treatments.
Figure 6. Effect of Se supplementation at 5, 10 and 20 µM on the leaf content of K (A), Na (B), Ca (C), K/Na ratio (D), S (E) and Se (F) of non-stressed and salt-stressed (50 mM NaCl) snap bean seedlings (28 days after sowing). The results are expressed as mean values of three measurements ± SE using Duncan’s multiple range test (p = 0.05). Different letters indicate significant differences among the treatments.
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Figure 7. Effect of Se supplementation at 5, 10 and 20 µM on the relative expression of sulfate transporter genes. Root-PvSULTR1 (A), Root-PvSULTR2 (B), Root-PvSULTR3 (C), Shoot-PvSULTR1 (D) Shoot-PvSULTR2 (E) and Shoot-PvSULTR3 (F) of non-stressed and salt-stressed (50 mM NaCl) snap bean seedlings (28 days after sowing). The results are expressed as mean values of three measurements ± SE using Duncan’s multiple range test (p = 0.05). Different letters indicate significant differences among the treatments.
Figure 7. Effect of Se supplementation at 5, 10 and 20 µM on the relative expression of sulfate transporter genes. Root-PvSULTR1 (A), Root-PvSULTR2 (B), Root-PvSULTR3 (C), Shoot-PvSULTR1 (D) Shoot-PvSULTR2 (E) and Shoot-PvSULTR3 (F) of non-stressed and salt-stressed (50 mM NaCl) snap bean seedlings (28 days after sowing). The results are expressed as mean values of three measurements ± SE using Duncan’s multiple range test (p = 0.05). Different letters indicate significant differences among the treatments.
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Figure 8. Effect of Se supplementation at 5, 10 and 20 µM on relative expression of salt stress responsive genes. SOS1 (A), NHX1 (B) and Osmotin (C) of non-stressed and salt-stressed (50 mM NaCl) snap bean seedlings (28 days after sowing). The results are expressed as mean values of three measurements ± SE using Duncan’s multiple range test (p = 0.05). Different letters indicate significant differences among the treatments.
Figure 8. Effect of Se supplementation at 5, 10 and 20 µM on relative expression of salt stress responsive genes. SOS1 (A), NHX1 (B) and Osmotin (C) of non-stressed and salt-stressed (50 mM NaCl) snap bean seedlings (28 days after sowing). The results are expressed as mean values of three measurements ± SE using Duncan’s multiple range test (p = 0.05). Different letters indicate significant differences among the treatments.
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Figure 9. Simplified model for the suggested effects of applied Se on snap bean plants grown under salinity stress. RWC, relative water content; MDA, malondialdehyde; FAA, free amino acids; G-POX, Guaiacol peroxidases; CAT, catalase; APX; ascorbate peroxidase; SOD, superoxide dismutase; blue solid lines indicate the positive effects of applied Se at low concentration; red dotted lines indicate the negative effects of applied Se at high level; green up arrow, increase; red down arrow.
Figure 9. Simplified model for the suggested effects of applied Se on snap bean plants grown under salinity stress. RWC, relative water content; MDA, malondialdehyde; FAA, free amino acids; G-POX, Guaiacol peroxidases; CAT, catalase; APX; ascorbate peroxidase; SOD, superoxide dismutase; blue solid lines indicate the positive effects of applied Se at low concentration; red dotted lines indicate the negative effects of applied Se at high level; green up arrow, increase; red down arrow.
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Table
Table 1. Oligonucleotide primer pairs used for quantitative RT-PCR analysis.
Table 1. Oligonucleotide primer pairs used for quantitative RT-PCR analysis.
Gene NameSequence
SULTR1F5′-CGCAGACTATGAATACCCGA-3′
R5′-TTCCTAAACGGGTCATCTGG-3′
SULTR2F5′-CAGAAGGAATAGCAATAGGA-3′
R5′-CAAGTAGCAGGAAGTAAAAG-3′
SULTR3F5′-TCTTTCTCACGGTCAGCAGT-3′
R5′-TAGCATTTGGAGTGTATTCG-3′
SOS1F5′-ACTTGCAGGAGGAATACAAC-3′
R5′-CGAGAAGAGAAGACCACATC-3′
OsmotinF5′-GAACGGAGGGTGTCACAAAATC-3′
R5′-CGTAGTGGGTCCACAAGTTCCT-3′
NHX1F5′-CGTGATGTCGCATTACACCT-3′
R5′-CTGGCAAACTCCCACTTCTC-3′
GAPDHF5′-TGACGACATCAAGAAGGTGGTG-3′
R5′-GAAGGTGGAGGAGTGGGTGTC-3′
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Farag, H.A.S.; Ibrahim, M.F.M.; El-Yazied, A.A.; El-Beltagi, H.S.; El-Gawad, H.G.A.; Alqurashi, M.; Shalaby, T.A.; Mansour, A.T.; Alkhateeb, A.A.; Farag, R. Applied Selenium as a Powerful Antioxidant to Mitigate the Harmful Effects of Salinity Stress in Snap Bean Seedlings. Agronomy 2022, 12, 3215. https://doi.org/10.3390/agronomy12123215

AMA Style

Farag HAS, Ibrahim MFM, El-Yazied AA, El-Beltagi HS, El-Gawad HGA, Alqurashi M, Shalaby TA, Mansour AT, Alkhateeb AA, Farag R. Applied Selenium as a Powerful Antioxidant to Mitigate the Harmful Effects of Salinity Stress in Snap Bean Seedlings. Agronomy. 2022; 12(12):3215. https://doi.org/10.3390/agronomy12123215

Chicago/Turabian Style

Farag, Hoda A. S., Mohamed F. M. Ibrahim, Ahmed Abou El-Yazied, Hossam S. El-Beltagi, Hany G. Abd El-Gawad, Mohammed Alqurashi, Tarek A. Shalaby, Abdallah Tageldein Mansour, Abdulmalik A. Alkhateeb, and Reham Farag. 2022. "Applied Selenium as a Powerful Antioxidant to Mitigate the Harmful Effects of Salinity Stress in Snap Bean Seedlings" Agronomy 12, no. 12: 3215. https://doi.org/10.3390/agronomy12123215

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