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Article

Positive Interaction of Selenium Nanoparticles and Olive Solid Waste on Vanadium-Stressed Soybean Plant

by
Mha Albqmi
1,2,
Mohammad Yaghoubi Khanghahi
3,*,
Samy Selim
4,
Mohammad M. Al-Sanea
5,
Taghreed S. Alnusaire
6,
Mohammed S. Almuhayawi
7,
Soad K. Al Jaouni
8,
Shaimaa Hussein
9,
Mona Warrad
10 and
Hamada AbdElgawad
11
1
Department of Chemistry, College of Science and Arts, Jouf University, Al Qurayyat 77447, Saudi Arabia
2
Olive Research Center, Jouf University, Sakaka 72341, Saudi Arabia
3
Department of Soil, Plant and Food Sciences, University of Bari Aldo Moro, Via Amendola 165/A, 70126 Bari, Italy
4
Department of Clinical Laboratory Sciences, College of Applied Medical Sciences, Jouf University, Sakaka 72341, Saudi Arabia
5
Department of Pharmaceutical Chemistry, College of Pharmacy, Jouf University, Sakaka 72341, Saudi Arabia
6
Department of Biology, College of Science, Jouf University, Sakaka 72341, Saudi Arabia
7
Department of Medical Microbiology and Parasitology, Faculty of Medicine, King Abdulaziz University, Jeddah 21589, Saudi Arabia
8
Department of Hematology/Oncology, Yousef Abdulatif Jameel Scientific Chair of Prophetic Medicine Application, Faculty of Medicine, King Abdulaziz University, Jeddah 21589, Saudi Arabia
9
Department of Pharmacology, College of Pharmacy, Jouf University, Sakaka 72341, Saudi Arabia
10
Department of Clinical Laboratory Sciences, College of Applied Medical Sciences at Al Qurayyat, Jouf University, Al Qurayyat 77454, Saudi Arabia
11
Department of Botany and Microbiology, Faculty of Science, Beni-Suef University, Beni-Suef 62521, Egypt
 
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*
Author to whom correspondence should be addressed.
Agriculture 2023, 13(2), 426; https://doi.org/10.3390/agriculture13020426
Submission received: 17 January 2023 / Revised: 7 February 2023 / Accepted: 9 February 2023 / Published: 10 February 2023
(This article belongs to the Special Issue Crop Antioxidant System and Its Responses to Stress)
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Abstract

:
The purpose of the current study was to determine the possible improvement in soybean plants’ tolerance against vanadium-induced stress in response to the application of olive solid waste (OSW) and selenium nanoparticles (Se-NPs), by assessing metabolites and plant defense systems. Drawing upon this aim, a pot experiment was performed where the soybean plants were grown with a fertilization treatment (including, control, OSW, Se-NPs, and Se-NPs + OSW) under vanadium stress (including non-stress and 350 mg sodium orthovanadate per kg of soil). Enhancement of hydrogen peroxide (H2O2) and malondialdehyde (MDA) accumulation in vanadium-stressed plants confirmed the oxidative damage in unfertilized plants. Results indicated the positive effects of the combined treatment (Se-NPs + OSW) in improving the plant stress tolerance by causing a balance in the produced ROS and detoxified ROS in the plant. It was mainly stimulated through the improvement of the photosynthetic parameters, anthocyanin metabolism pathway, phenylpropanoid pathway, non-enzymatic antioxidant metabolites (tocopherols, malondialdehyde, polyphenols, and flavonoids), antioxidant enzymes, and biochemical components involved in the ASC/GSH cycle (ascorbate, ascorbate peroxidase, dehydroascorbate reductase, monodehydroascorbate reductase, glutathione, glutathione reductase, and glutathione peroxidase), and antioxidant direct scavenging enzymes (peroxidase, catalase, and superoxide dismutase), which finally resulted in higher plant biomass. In conclusion, the simultaneous application of OSW and Se-NPs treatments provided a reliable protection for soybean plants in vanadium-contaminated soils through the activation of antioxidant and non-antioxidant defense mechanisms.

1. Introduction

Vanadium (V), as a potentially dangerous heavy metal, has widely polluted the soil and environment due to its extensive release from various industrial processes, fertilizers, the combustion of coals and oils, etc. [1]. Although some metal elements (e.g., vanadium) are involved in some vital biochemical processes in plants, they can be toxic to plants and humans at concentrations exceeding the safe threshold [2]. The concentration of vanadium in the soil usually varies from 10 to 400 µg g−1 (average of 90 µg g−1), which can be, in particular, uptaken by plants as vanadate anion (H2VO4−) in competing with the structurally analogous H2PO4− in place of phosphate [3]. The toxic impacts of vanadium on plants, e.g., originating oxidative stress, hindering plant growth, and repressing the uptake of essential nutrients, occur when the concentration of this element in the plant reaches more than 2 µg g−1 of plant biomass [4]. In this regard, one of the most significant adverse effects of this potentially toxic element on crop plants is the loss of fresh and dry biomass, which can be a subsequence of lowering translocation from root to shoot [5,6]. In addition, a substantial increment in the hydrogen peroxide (H2O2) and malondialdehyde (MDA) content caused severe oxidative damage in crops in response to vanadium toxicity [7], which in turn vastly activated the enzymatic and non-enzymatic components of the antioxidant defense system in plants [6].
One major concern, that has dominated the field of agricultural sustainability for many years, is finding the best strategies for the management of soil fertility and plant nutrients in replacing synthetic fertilizers, while a remarkable underscore on the recovery and recycling of food by-products and wastes [8,9,10]. Recently, research has emerged that offers findings about olive solid waste (OSW), which is generated by the olive oil manufacturing process [11], as a source of optimum nutritional value compounds to generate an organic fertilizer. The controversy about scientific evidence for the positive effects of OSW on plants has raged unabated for years, especially since some characteristics of olive waste are favorable for the sustainable agriculture section because of its enrichment in organic matter (including fiber, lignin, uronic acids, and polyphenolic compounds; >1 g l−1) [12], N (~1 g l−1), P (~0.2 g l−1), K (>4 g l−1), and Mg (~0.1 g l−1) [13] and its antimicrobial and antiviral properties [8].
Selenium (Se) deficiency, as an essential micronutrient, is one of the leading human health concerns, and the cause of the rising risks of many diseases and cancers [14]. Therefore, Se fertilizers play an important role in the maintenance of Se levels in an adequate range in crops, since Se dietary uptake from crop-source products is the major fountainhead of Se for humans [15]. The high bioavailability and mobility of Se traditional fertilizers (e.g., SeO32–) is a classic problem in environmental safety [16], which led researchers to introduce a new form of Se supplements named selenium nanoparticles (Se-NPs) with a much higher efficiency and lower toxicity [14]. The use of Se-NP fertilizer has especially received considerable critical attention because of its positive effects on plant growth under stressful conditions, confirming its association with plant oxidative stress tolerance [17,18].
Nevertheless, much uncertainty still exists about the effects of OSW and Se-NPs on plants under potentially toxic elements. Therefore, the key research questions of this study were whether the application of OSW and Se-NPs, alone or as a combined treatment, can (i) improve the antioxidant (enzymatic and non-enzymatic) and non-antioxidant defense system in soybean (Glycine max L.) plants, and (ii) enhance the soybean seedlings biomass under vanadium stress, or not.

2. Materials and Methods

2.1. Plant Materials and Experimental Setup

A pot experiment was conducted in a completely randomized design with three replications; 24 pots were used in this experiment (4 fertilization levels × 2 vanadium stress levels × 3 replications). Healthy soybean seeds (var. Giza 112) were surface sterilized by soaking them for 5 min in a sodium hypochlorite solution (5% v/v), washed several times with sterile water, planted into 2 L pots containing soil and sterilized sand (1:2), and stratified into potting mix (Tref EGO substrates, Moerdijk, the Netherlands). Plants were kept for 6 weeks after sowing (DAS) in controlled-environment chambers with a constant light/temperature regime (16 h light at 26 °C, and 8 h dark at 18 °C).

2.2. Application of Treatments

Fertilization treatment was used at four levels, including (i) no fertilization control (Co), (ii) olive solid waste (OSW), (iii) selenium nanoparticles (Se-NPs), and (iv) a combined treatment (OSW + Se-NPs). OSW was applied to the pots (a rate of 4% w/w), after collecting from a traditional, and air-drying for one month before use [19,20]. The physicochemical characteristics of OSW are given in Table 1.
Se-NPs (American Elements, Los Angeles, CA, USA) were also applied by priming the seeds in a suspension containing 25 mg L−1 of selenium nanoparticles for 10 h with continuous shaking (IKA KS 501 shaker, Staufen, Germany) at room temperature, and washing thrice with distilled water for 2 min. Se-NPs were already sonicated to avoid the coarse aggregate in the aqueous suspension [21]. According to the manufacturer’s data, Se-NPs are gray to black solid particles with a purity of 99.99% and a density of 4.79 g cm−3. A scanning electron microscope (SEM manufactured by JEOL JSM-6510, LA, Japan) was also used to validate the morphological features of the Se-NP structure. The dose of applied concentration of OSW and Se-NPs were selected based on our preliminary experiments testing different concentrations of solid OSW (0, 2, 4, 6, 8, and 10%, w/w) and Se-NPs (0, 10, 25, 50, and 75 mg L−1) on different crop growth.
Two levels of vanadium stress included non-stress (control) and vanadium stress. Accordingly, a dose of 350 mg sodium orthovanadate (Na3VO4: Sigma-Aldrich, Steinheim am Albuch, Germany, 99.98% trace metals basis) per kg of soil was added to the soil mixture in pots to induce vanadium stress, based on preliminary experiments as it induces a reduction in growth by approximately 50% [22].

2.3. Sampling

2.3.1. Determination of Plant Biomass, Photosynthetic Capacity and Pigments

Plant shoot tissues were collected at 6 weeks DAS (V5 growth stage) and kept at −80 °C for subsequent biochemical analysis. Moreover, the fresh and dried weight of the shoots were calculated.
The fully developed leaves of the soybean plants were used for the non-destructive measuring of the photosynthesis rate (μmol CO2 m−2 s−1) using the LI-COR portable photosynthesis system (LI-COR 6400/XT, LI-COR, Nebraska, USA). Fresh samples of leaves (1.0 cm2) were also used to measure the photosynthesis pigments, including chlorophyll a, chlorophyll b, and the carotenoid content based on a modified Porra [23] method [24].

2.3.2. Assessment of Stress Biomarkers, Antioxidant Metabolites, and Antioxidant Enzyme Activities

Leave samples were used to determine the accumulation of malondialdehyde (MDA) and hydrogen peroxide (H2O2). Accordingly, 50 mg of samples was homogenized in 1 mL of ethanol (80% v/v) using a MagNA Lyser (Roche, Vilvoorde, Belgium). After centrifugation, the extracted supernatant was tested using the thiobarbituric acid assay, and the absorbance was measured at 440, 532, and 600 nm using a micro-plate reader (Synergy Mx, Biotek Instruments Inc., Vermont, VT, USA). The xylenol orange method, which relies on peroxide-catalyzed oxidation of Fe2+, was also used to measure H2O2 content in trichloroacetic acid (0.1%) [25].
Total antioxidant capacity (ferric-reducing antioxidant power) was extracted in ice-cold 80% ethanol using a MagNA Lyser and measured using Trolox as a reference base on using the ferric-reducing antioxidant power (FRAP) method [21]. Plant materials were extracted in 80% ethanol using MagNALyser for ascorbate and glutathione measurement (Roche, Vilvoorde, Belgium). HPLC was used to measure reduced ascorbate (ASC) and reduced glutathione (GSH). Polyphenols and flavonoids (including anthocyanins) were extracted by homogenizing the fresh plant materials in 80% ethanol and centrifuged for 15 min at 5000 rpm. The clear extract was then used to determine the total phenolic and flavonoid content using the Folin–Ciocalteu and aluminum chloride tests [25,26]. To measure the tocopherols content, plant materials were extracted in n-hexane solvent and quantified using HPLC (Shimadzu, Hertogenbosch, the Netherlands), and analyzed by Shimadzu Class VP 6.14 software provided by the HPLC system, based on the methods described by AbdElgawad et al. [27], in which dimethyl tocol (DMT; 5 ppm) was used as an internal standard.
Samples were homogenized in 1 mL buffer [50 mM potassium phosphate, pH 7.0, 10% (w/v) polyvinyl pyrrolidone (PVP), 0.25% (v/v) Triton X-100, 1 mM phenylmethylsulfonyl fluoride (PMSF), 1 mM ASC]. After centrifugation, the clear supernatant was used to assess the activities of superoxide dismutase (SOD, EC 1.15.1.1), peroxidase (POX, EC 1.11.1), catalase (CAT, EC1.11.1.6), glutathione peroxidase (GPX, EC 1.11.1.9), and ascorbate peroxidase (APX, GST, EC 2.5.1.18). Dhindsa et al. [28] evaluated SOD activity by measuring the inhibition of nitroblue tetrazolium (NBT) reduction at 560 nm. POX activity was evaluated using the technique developed by [29] based on pyrogallol oxidation. The breakdown of H2O2 at 240 nm was used to assess CAT activity [30]. The quantification of APX, MDHAR, DHAR, and GR activities was fully described by Murshed et al. [31]. GPX activity was also measured according to a reduction in NADPH absorption at 340 nm [32].

2.4. Statistical Analysis

All statistical analyses, including a two-way analysis of variance (ANOVA) and Tukey HSD (honestly significant difference) test, as well as drawing the graphs, were performed using the SigmaPlot software. The results were expressed as mean ± standard deviation.

3. Results

The results obtained from the analysis of some photosynthetic parameters can be compared in Figure 1. Accordingly, strong evidence of the positive effects of selenium nanoparticles and olive solid waste (Se-NPs, OSW, and Se-NPs + OSW) treatments on photosynthetic capacity was found when the plants were exposed to vanadium stress, which were 4.5, 4.3, and 10.2 times higher than those in the control plants under stress, respectively. Moreover, the photosynthetic capacity of plants treated by Se-NPs + OSW under stress (7.6 µmol CO2 m−2 s−1) was statistically placed in a same group with no fertilization (8.1 µmol CO2 m−2 s−1) and Se-NPs + OSW (9.5 µmol CO2 m−2 s−1) in a non-stress condition (Figure 1). Almost the same findings were observed for chlorophyll a, b, and a + b concentrations, confirming the greater effect of the combined treatment (Se-NPs + OSW) in stress conditions, which were not significantly different from the fertilization levels in non-stress conditions (Figure 1).
Since the concentration of carotenoids in fertilization treatments did not increase in stressed plants (Figure 1), we decided to measure the changes in the anthocyanin content and parameters related to its metabolism, since anthocyanins and carotenoids are considered the main pigments involved in a plant’s protection from stress. Figure 2 is quite revealing regarding the increment in all studied parameters of anthocyanin metabolism in response to OSW and Se-NPs + OSW treatments under vanadium stress. In this regard, the highest concentration of anthocyanin, chalcone synthase, and naringenin was observed in Se-NPs + OSW treatment in stressed plants, which were approximately +57, +29, and +58% higher than those in unfertilized stressed plants, respectively (Figure 2). Figure 2 also shows an overview of the concentration of key enzymes in the phenylpropanoid pathway, which is an important defense response of plant cells under stress. Similarly, the maximum concentration of phenylalanine ammonia-lyase, cinnamic acid, and phenylalanine was found in Se-NPs + OSW treatment in vanadium-induced stress, which was approximately +47, +54, and +71% greater than those in no fertilization treatment in the non-stress condition, respectively (Figure 2).
Then, we measured the antioxidant defense system, including some enzymatic and non-enzymatic components, to have a clear idea about their possible changes in protecting biological systems against vanadium-induced oxidative stress in plants. The most obvious finding to emerge from the analysis of oxidative markers (hydrogen peroxide and total antioxidant capacity) and non-enzymatic antioxidant metabolites (tocopherols, malondialdehyde, polyphenols, and flavonoids), where all studied parameters increased under vanadium stress (Figure 3). Although the highest content of H2O2 (equal to 1112 µg g−1) was significantly obtained from the no fertilization treatment under vanadium stress, its concentration was non-significantly higher in other fertilization levels in stressed plants than the same levels in the unstressed plants (Figure 3). A clear benefit of OSW-containing treatments (OSW and Se-NPs + OSW) in improving the levels of total antioxidant capacity, tocopherols, polyphenols, and flavonoids were found in plants treated by vanadium stress, which were significantly (p < 0.05) higher than those in other fertilization levels in both stress and non-stress conditions (Figure 3). OSW and Se-NPs + OSW treatments also kept the content of MDA in stressed plants at the level of non-stressed plants, in contrast to Se-NPs and no fertilization treatments, which were significantly higher (+49 and +108%, respectively) in stressed conditions than the same levels in non-stressed conditions (Figure 3).
Similarly, OSW and Se-NPs + OSW treatments significantly enhanced the levels of the antioxidant enzymes and metabolites involved in the ascorbate-glutathione (ASC/GSH) cycle in stressed plants, which were in particular higher than unfertilized plants under stress at approximately +31 and +54% for ascorbate, +210 and +113% for ascorbate peroxidase, +68 and +46% for dehydroascorbate reductase, +63 and +41% for monodehydroascorbate reductase, +126 and +89% for glutathione, +324 and +272% for glutathione reductase, and +131 and +135% for glutathione peroxidase, respectively (Table 2).
In contrast, the increment in the antioxidant direct scavenging enzymes levels has been made in the selenium nanoparticles-containing treatments (Se-NPs and Se-NPs + OSW) in stressed plants, which were significantly (p < 0.05) greater than those in the other treatments in both the stress and non-stress conditions (Table 3). The maximum concentration for the peroxidase, catalase, and superoxide dismutase enzymes was related to the Se-NPs + OSW, Se-NPs + OSW, and Se-NPs treatments in stressed plants, respectively, which were 2.2, 2.9, and 1.5 times higher than those in unfertilized stressed plants, respectively (Table 3).
From Figure 4, it can be seen that by far the greatest improvement in vanadium stress tolerance in the Se-NPs + OSW treatment resulted in a higher biomass in the stressed plants. Accordingly, the maximum amount of fresh weight and dry weight of plants under stress was found in plants treated by Se-NPs + OSW, which was placed in the same statistical group with all fertilization levels in non-stress conditions (Figure 4).

4. Discussion

The present study set out with the aim of assessing the possible effects of selenium nanoparticles and olive solid waste in stimulating plant tolerance to vanadium stress. What is clear from the results is that vanadium contamination negatively affected almost all biochemical and metabolic parameters in unfertilized soybean seedlings. One of the most dependent parameters on vanadium stress was the photosynthesis parameters. Their decreases under heavy metal stress were already reported in association with disrupting photosynthetic electron transport chain function, increasing the content of reactive oxygen species (ROS) in chloroplasts, subsequently disorganizing photosynthesis pigment synthesis [33,34]. However, this experiment also did not detect any strong evidence for improving photosynthesis parameters in unstressed plants; both Se-NPs and OSW were found to cause an increment in photosynthesis capacity and chlorophyll pigments content under vanadium stress, in particular, when the combined treatment (Se-NPs + OSW) was applied. This finding agrees with the findings of Ghidaoui et al. [35], Magdich et al. [36], and Kamali-Andani et al. [37], who reported increasing the photosynthesis capacity and pigments content in response to selenium nanoparticles and olive waste under potentially toxic element stress.
Drawing upon not increasing the carotenoid concentration in response to OSW and Se-NPs in Figure 1, this study attempted to ascertain the anthocyanin synthesis and metabolism, as another key photo-protectant. The most surprising aspect of the data was the decrement in anthocyanin content when exposed to Se-NPs (non-significantly in non-stress and significantly under stress) as compared to the control plants. As can be seen from Figure 2, it can be concluded that with the reduction of the chalcone synthase enzyme, as the key and initial rate-limiting enzyme of the flavonoid biosynthesis pathway [38] in reaction to selenium, the mediation synthesis of naringenin was also negatively affected, which resulted in the reduction of the biosynthesis of anthocyanin (Figure 2) and flavonoid (Figure 3) content. However, this finding does not support the previous research showing the stress-protective property of selenium by improving the anthocyanin accumulation in stressed plants [39]. The highest amount of anthocyanin, chalcone synthase, and naringenin was obtained from the combined treatment (Se-NPs + OSW), which somehow indicated the positive effect of Se-NPs on anthocyanin biosynthesis when the OSW treatment was used and showed the synergistic effect of these treatments in the simultaneous application.
Inducing phenylalanine ammonia-lyase accumulation in stressed plants (Figure 2) seems to be consistent with other researchers who found similar findings under several biotic and abiotic stresses, in particular heavy metal stress [40,41]. The results also indicated the enhancement of the components of the phenylpropanoid pathway, including phenylalanine ammonia-lyase, cinnamic acid, and phenylalanine, in response to OSW-containing treatments under vanadium stress (Figure 2). One of the main differences between OSW and Se-NP treatments on vanadium-stressed plants can be explained in part by being more effective of OSW in activating phenylalanine ammonia-lyase in plants, which is a strong antioxidant system in balancing between generated ROS and detoxified ROS, as well as being responsible for phenolic compound biosynthesis [42], a mechanism that did not respond to the application of Se-NPs. Therefore, the activation of phenylalanine ammonia-lyase could be a major factor, if not the only one, causing the enhancement of polyphenol content in OSW-treated plants under stress, as shown in Figure 3. Furthermore, the increment of phenylalanine ammonia-lyase accumulation led to an increase in cinnamic acid and phenylalanine content in our research, since this enzyme is involved in the activation of the production of cinnamic acid by catalyzing the phenylalanine as the first step in the phenylpropanoid pathway and the main adjustment phase between primary and secondary metabolism [41,42].
From Figure 3, it can be seen that by far the greatest accumulation of hydrogen peroxide (H2O2) and malondialdehyde (MDA) was obtained from no fertilization in vanadium-stressed plants. In the same vein, Roychoudhury [6] and Imtiaz et al. [7] reported increments in H2O2 and MDA accumulation in the leaf, stem, and root tissues of plants under vanadium-induced stress that altogether resulted in severe oxidative damage. On the other hand, a decrement in H2O2 and MDA concentration in plants exposed to Se-NPs and OSW compared to unfertilized plants under stress (Figure 3). However, no previous study has investigated the effect of OSW on these oxidative stress markers, the compensatory impacts of Se to preserve the cell membranes against oxidative damage was already documented [37,43]. It seems that the higher detoxification of H2O2 and MDA in fertilized plants under vanadium-induced stress are due to the higher activation of antioxidant enzymes involved in ASC/GSH cycle (ASC, APX, DHAR, MDHAR, GSH, GR, and GPX) in response to OSW-containing treatments, and a direct scavenging pathway (POX, SOD, and CAT) when exposed to Se-NP-containing treatments, as shown in Table 2 and Table 3. The evidence for the relationship between detoxifying excess ROS and reinforcing the antioxidant defense system was previously proved [19,37].
Although the differential responses of enzymes involved in the ASC/GSH cycle to various heavy metals stress have previously been reported [44], in our study, it has even responded differently to Se-NPs and OSW treatments. However, the activation of the ASC/GSH cycle was not observed in Se-NP-treated plants and these results should be interpreted with caution, especially since the interaction between this antioxidant pathway and other signaling molecules or any other molecules in oxidative stress is not well understood [44]. A possible explanation for this might be the vulnerability of the components of the ASC/GSH cycle to oxidative damage, despite their protective role in maintaining the cellular components from oxidative damage, which can subsequently affect their antioxidant defense under stress [44]. It seems that the increase of other non-enzymatic antioxidants in OSW-treated plants in our experiment, such as tocopherols, total antioxidant capacity (ferric-reducing antioxidant power), and flavonoids (Figure 3) led to the synergistic effect of the ASC/GSH pathway in the detoxification of ROS, an interaction that was not observed in Se-NP-treated plants. El-Badri et al. [45] related this difference in the plant’s reaction to Se-NPs to its slow uptake by the plant and its rapid oxidation to selenite in plant cells. Our results illustrate the mechanism of Se-NP-treated plants upon exposure to vanadium stress (Table 3), in which the antioxidant direct scavenging enzymes (POX, CAT, and SOD) significantly increased as compared to OSW and no fertilization treatments. Similarly, Feng et al. [46] and Kamali-Andani et al. [37] reported that the maintenance of cellular homeostasis and the regulating of ROS detoxification was associated with a sharp increment in POX, CAT, and SOD accumulation in Se-NP-treated plants.
The increment of plant fresh and dry weight in response to OSW and Se-NPs under stress is consistent with the findings of Mohawesh et al. [47] and Belaqziz et al. [19]. As can be seen from Figure 4, the simultaneous use of OSW and Se-NP treatments were clearly cooperative and complementary to stimulate biomass accumulation in soybean plants in coping with vanadium stress in contaminated soils.

5. Conclusions

In conclusion, the most significant finding to emerge from this research was the significant impact of the combined treatment of olive solid waste and selenium nanoparticles (Se-NPs + OSW) in improving the plant stress tolerance by causing a balance in the produced ROS from oxidative damages resulting from vanadium stress and detoxified ROS in the plant. It was mainly stimulated through the activation and improvement of the photosynthetic parameters, anthocyanin metabolism pathway, phenylpropanoid pathway, non-enzymatic antioxidant metabolites (tocopherols, malondialdehyde, polyphenols, and flavonoids), antioxidant enzymes and biochemical components involved in the ASC/GSH cycle (ascorbate, ascorbate peroxidase, dehydroascorbate reductase, monodehydroascorbate reductase, glutathione, glutathione reductase, and glutathione peroxidase), and antioxidant direct scavenging enzymes (peroxidase, catalase, and superoxide dismutase), which finally resulted in a higher plant biomass. Therefore, the evidence from this study suggested that the simultaneous application of OSW and Se-NP treatments could be recommended for the fertilizations/supplementations of soybean cultivation in areas that have been exposed to vanadium stress, the positive features that have not been found when using either of these treatments separately, at least not as much as with the combined treatment. This is the first study reporting the beneficial and synergistic effects of OSW and Se-NPs under stress. Nevertheless, since the generalizability of these results is subject to certain limitations, such as not specifically evaluating the accumulation of vanadium, selenium, and nutrients in plant tissues, a number of possible future studies using the same experimental setup are apparent.

Author Contributions

Conceptualization, M.A. and S.S.; methodology, M.M.A.-S. and T.S.A.; software, M.Y.K. and S.K.A.J.; validation, S.H. and M.S.A.; formal analysis, H.A. and M.W.; investigation, M.A. and M.S.A.; resources, M.A and S.S.; data curation, M.Y.K., T.S.A., and M.W.; writing—original draft preparation, M.Y.K.; writing—review and editing, M.Y.K., M.A. and H.A.; visualization, S.S.; supervision, M.Y.K., S.S., and H.A.; project administration, M.A., S.S. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by the Deanship of Scientific Research in cooperation with Olive Research Center at Jouf University (Grant Number: DSR2022-RG-0167).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The data presented in this study are available upon request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

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Agriculture 13 00426 g001 550
Figure 1. The effect of olive solid waste (OSW) and selenium nanoparticles (Se-NPs) on the photosynthesis rate and photosynthetic pigments in plants under vanadium stress. Means in each parameter followed by similar letter(s) are not significantly different at 5% probability level (Tukey test).
Figure 1. The effect of olive solid waste (OSW) and selenium nanoparticles (Se-NPs) on the photosynthesis rate and photosynthetic pigments in plants under vanadium stress. Means in each parameter followed by similar letter(s) are not significantly different at 5% probability level (Tukey test).
Agriculture 13 00426 g001
Agriculture 13 00426 g002 550
Figure 2. The effect of olive solid waste (OSW) and selenium nanoparticles (Se-NPs) on the components of anthocyanin metabolism and phenylpropanoid pathway in plants under vanadium stress. Means in each parameter followed by similar letter(s) are not significantly different at 5% probability level (Tukey test). PAL: Phenylalanine ammonia lyase (PAL); CA: Cinnamic acid; CHS: Chalcone synthase; PA: Phenylalanine.
Figure 2. The effect of olive solid waste (OSW) and selenium nanoparticles (Se-NPs) on the components of anthocyanin metabolism and phenylpropanoid pathway in plants under vanadium stress. Means in each parameter followed by similar letter(s) are not significantly different at 5% probability level (Tukey test). PAL: Phenylalanine ammonia lyase (PAL); CA: Cinnamic acid; CHS: Chalcone synthase; PA: Phenylalanine.
Agriculture 13 00426 g002
Agriculture 13 00426 g003 550
Figure 3. The effect of olive solid waste (OSW) and selenium nanoparticles (Se-NPs) on the oxidative biomarkers and antioxidant metabolites in plants under vanadium stress. Means in each parameter followed by similar letter(s) are not significantly different at 5% probability level (Tukey test). TAC: Total antioxidant capacity; Toc: Tocopherols; MDA: Malondialdehyde; POL: Polyphenols; Flav: Flavonoids.
Figure 3. The effect of olive solid waste (OSW) and selenium nanoparticles (Se-NPs) on the oxidative biomarkers and antioxidant metabolites in plants under vanadium stress. Means in each parameter followed by similar letter(s) are not significantly different at 5% probability level (Tukey test). TAC: Total antioxidant capacity; Toc: Tocopherols; MDA: Malondialdehyde; POL: Polyphenols; Flav: Flavonoids.
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Agriculture 13 00426 g004 550
Figure 4. The effect of olive solid waste (OSW) and selenium nanoparticles (Se-NPs) on the plant biomass under vanadium stress. Means in each parameter followed by similar letter(s) are not significantly different at 5% probability level (Tukey test).
Figure 4. The effect of olive solid waste (OSW) and selenium nanoparticles (Se-NPs) on the plant biomass under vanadium stress. Means in each parameter followed by similar letter(s) are not significantly different at 5% probability level (Tukey test).
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Table
Table 1. Measurement of basic physicochemical parameters (±standard deviation) of olive solid waste.
Table 1. Measurement of basic physicochemical parameters (±standard deviation) of olive solid waste.
Basic characeristics
Water content (%)117.15 ± 4.11
Dry matter (%)12.49 ± 1.1
pH5.06 ± 0.10
Electric conductivity (mS cm−1)18.1± 0.23
Chemical oxygen demand (g L−1)111.08 ± 7.1
Biochemical oxygen demand (g L−1)60.02 ± 4.14
Organic matter (g L−1)65.02 ± 8.04
Salinity (g L−1)3.09 ± 0.2
Minerals
Nitrogen (g L−1)5.22 ± 0.1
Phosphorus (g L−1)3.86 ± 0.21
Potassium (g L−1)11.51 ± 1.01
Calcium (g L−1)1.50 ± 0.04
Magnesium (g L−1)1.23 ± 0.32
Sodium (g L−1)2.30 ± 0.1
Chloride (g L−1)2.08 ± 0.41
Fe (g L−1)1.10 ± 0.12
Zn (g L−1)0.60 ± 0.1
Antioxidants
Antioxidant activity (FRAP)51.92 ± 2.10
Antioxidant activity DPPH (%)47.38 ± 1.07
Total phenols (g L−1)10.21 ± 1.09
Flavonoids (g L−1)1.05 ± 0.09
Table
Table 2. The effect of olive solid waste (OSW) and selenium nanoparticles (Se-NPs) on the components of ASC/GSH cycle in plants under vanadium stress.
Table 2. The effect of olive solid waste (OSW) and selenium nanoparticles (Se-NPs) on the components of ASC/GSH cycle in plants under vanadium stress.
ASCAPXDHARMDHARGSHGRGPX
Non-stressControl0.22 ± 0.02 c0.35 ± 0.06 c0.16 ± 0.02 b0.05 ± 0.00 c0.04 ± 0.00 c0.10 ± 0.02 cd0.52 ± 0.07 b
OSW0.20 ± 0.02 c0.32 ± 0.05 c0.15 ± 0.01 b0.05 ± 0.00 c0.04 ± 0.00 c0.13 ± 0.02 c0.50 ± 0.03 b
Se-NPs0.19 ± 0.02 c0.38 ± 0.05 c0.19 ± 0.02 b0.06 ± 0.00 bc0.05 ± 0.01 c0.08 ± 0.01 d0.53 ± 0.04 b
Se-NPs + OSW0.21 ± 0.02 c0.40 ± 0.07 c0.20 ± 0.02 b0.04 ± 0.00 c0.05 ± 0.00 c0.09 ± 0.01 d0.53 ± 0.07 b
Vanadium stressControl0.24 ± 0.02 bc0.42 ± 0.07 c0.21 ± 0.02 b0.05 ± 0.00 bc0.05 ± 0.01 c0.13 ± 0.02 c0.60 ± 0.07 b
OSW0.32 ± 0.03 a1.31 ± 0.11 a0.35 ± 0.04 a0.09 ± 0.00 a0.12 ± 0.01 a0.55 ± 0.05 a 1.39 ± 0.24 a
Se-NPs0.20 ± 0.02 c0.38 ± 0.05 c0.17 ± 0.02 b0.04 ± 0.00 c0.04 ± 0.00 c0.08 ± 0.01 d0.57 ± 0.08 b
Se-NPs + OSW0.37 ± 0.03 a0.90 ± 0.08 b0.30 ± 0.03 a0.08 ± 0.00 a0.10 ± 0.02 ab0.49 ± 0.06 b1.41 ± 0.19 a
Means in each row followed by similar letter(s) are not significantly different at 5% probability level (Tukey test). ASC: Ascorbate; APX: Ascorbate peroxidase; DHAR: Dehydroascorbate reductase; MDHAR: Monodehydroascorbate reductase; GSH: Glutathione; GR: Glutathione reductase; GPX: Glutathione peroxidase.
Table
Table 3. The effect of olive solid waste (OSW) and selenium nanoparticles (Se-NPs) on antioxidant direct scavenging enzymes in plants under vanadium stress.
Table 3. The effect of olive solid waste (OSW) and selenium nanoparticles (Se-NPs) on antioxidant direct scavenging enzymes in plants under vanadium stress.
POXCATSOD
Non-stressControl1.41 ± 0.21 c7.86 ± 0.83 c217.64 ± 25.10 c
OSW1.30 ± 0.09 c7.81 ± 0.84 c220.16 ± 17.38 c
Se-NPs0.97 ± 0.11 c8.91 ± 0.91 c242.66 ± 18.87 c
Se-NPs + OSW1.30 ± 0.23 c8.40 ± 0.87 c231.69 ± 27.67 c
Vanadium stressControl1.52 ± 0.21 c9.50 ± 0.97 c264.64 ± 25.71 c
OSW1.44 ± 0.22 c8.79 ± 0.95 c255.70 ± 30.36 c
Se-NPs2.43 ± 0.31 b21.22 ± 3.04 b404.53 ± 29.19 a
Se-NPs + OSW3.43 ± 0.35 a27.73 ± 3.53 a337.50 ± 32.74 ab
Means in each row followed by similar letter(s) are not significantly different at 5% probability level (Tukey test). POX: Peroxidase; CAT: Catalase; SOD: Superoxide dismutase.
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Albqmi, M.; Yaghoubi Khanghahi, M.; Selim, S.; Al-Sanea, M.M.; Alnusaire, T.S.; Almuhayawi, M.S.; Al Jaouni, S.K.; Hussein, S.; Warrad, M.; AbdElgawad, H. Positive Interaction of Selenium Nanoparticles and Olive Solid Waste on Vanadium-Stressed Soybean Plant. Agriculture 2023, 13, 426. https://doi.org/10.3390/agriculture13020426

AMA Style

Albqmi M, Yaghoubi Khanghahi M, Selim S, Al-Sanea MM, Alnusaire TS, Almuhayawi MS, Al Jaouni SK, Hussein S, Warrad M, AbdElgawad H. Positive Interaction of Selenium Nanoparticles and Olive Solid Waste on Vanadium-Stressed Soybean Plant. Agriculture. 2023; 13(2):426. https://doi.org/10.3390/agriculture13020426

Chicago/Turabian Style

Albqmi, Mha, Mohammad Yaghoubi Khanghahi, Samy Selim, Mohammad M. Al-Sanea, Taghreed S. Alnusaire, Mohammed S. Almuhayawi, Soad K. Al Jaouni, Shaimaa Hussein, Mona Warrad, and Hamada AbdElgawad. 2023. "Positive Interaction of Selenium Nanoparticles and Olive Solid Waste on Vanadium-Stressed Soybean Plant" Agriculture 13, no. 2: 426. https://doi.org/10.3390/agriculture13020426

APA Style

Albqmi, M., Yaghoubi Khanghahi, M., Selim, S., Al-Sanea, M. M., Alnusaire, T. S., Almuhayawi, M. S., Al Jaouni, S. K., Hussein, S., Warrad, M., & AbdElgawad, H. (2023). Positive Interaction of Selenium Nanoparticles and Olive Solid Waste on Vanadium-Stressed Soybean Plant. Agriculture, 13(2), 426. https://doi.org/10.3390/agriculture13020426

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