Perspective Chapter: Enhancing Plant Resilience to Salinity Induced Oxidative Stress – Role of Exogenous Elicitors

Abstract

Plants face various abiotic stresses, among which soil salinity is a significant threat. It reduces plants’ growth and development remarkably due to its detrimental effects. Salt stress occurs when soluble salts accumulate in the soil solution. A considerable portion of the world’s soil is negatively impacted by salinity, even at low concentrations. Salinity can hinder plant physiological processes by inducing osmotic stress and ionic toxicity, generating excessive reactive oxygen species (ROS) and leading to oxidative stress within plant cells. The formation of ROS is a normal plant metabolic phenomenon, but excessive ROS-induced oxidative stress can disrupt membrane activities, enzymes, and cell walls, cause cell damage, and, in severe cases, plant death. Various strategies, such as chemical substances and plant growth-promoting substances, are applied exogenously to diminish ROS-induced oxidative stress. Additionally, the use of rhizobacteria that have plant growth-promoting traits, organic amendments, rhizospheric fungi, and various genetic approaches are considered when addressing salt stress in plants. These mechanisms for scavenging ROS enhance plants’ tolerance to saline stress by developing an antioxidant defense system, reducing oxidative damage at the cellular level, and maintaining ion homeostasis. This chapter focuses on the latest research regarding the alleviation of salinity-induced oxidative stress in several crops through the exogenous application of stress elicitors.

1. Introduction

The global community has become increasingly concerned about climate change, driven by global warming, and its adverse effects on the environment and agroecosystems. It is increasingly recognized that the objective of environmental sustainability is seriously threatened by global warming. Weather fluctuations due to climate change profoundly affect agriculture by interrupting planting and harvesting schedules, changing crop growth patterns, and increasing the prevalence of pests and pathogens, thereby jeopardizing crop yields and the food security of the world. Numerous environmental factors, including salinity, high temperatures, drought, heat waves, frost, cool temperatures, and high levels of carbon dioxide (CO₂), impact both annual and perennial plants [1].

Among these factors, salinity stress affects hectares of cultivable land worldwide, and its severity is expected to escalate further as a consequence of climate change. Salinity adversely affects over 1 billion hectares of land, damaging 20% of irrigated cultivable land [2, 3]. The excessive accumulation of salts has a detrimental consequence on plant growth, development, seed performance, and other plant properties due to stress caused by salt. Sources of salt in the soil include seawater intrusion, inherent soil salinity, poor drainage, plant transpiration, seawater sprays, wind-borne salts, surface evaporation, excessive fertilizer use, soil additives, sewage sludge, and industrial brine dumping. According to the Food and Agriculture Organization [4], around 833 million hectares of subsoil (30–100 cm) and 424 million hectares of topsoil (0–30 cm) are disrupted by salt in 118 nations or 85% of the world’s land surface. Of the topsoil damaged by salt, 10% are sodic, 5% are saline-sodic, and 85% are saline.

Generally, soil salinity refers to the existence of an abundant amount of soluble salts within a particular area. When the soil’s electrical conductivity (EC) value is 4 dS m⁻¹ or more, it is considered saline soil [5]. Soil solutions usually contain soluble salts such as sodium sulfate (Na₂SO₄) and sodium chloride (NaCl), although there are also partially soluble salts, including calcium sulfate (CaSO₄), and even magnesium sulfate (MgSO₄) with low solubility, sodium bicarbonate (NaHCO₃), potassium nitrate (KNO₃), and many others. The primary increase in salinity essentially involves Na⁺ and Cl⁻ ions. Although both Na⁺ and Cl⁻ ions are toxic to plants, the Cl⁻ ion poses a more significant threat [6, 7]. These ionic imbalances in soil pose a burgeoning problem for agriculture that needs irrigation, significantly constraining crop productivity and dictating their spatial distribution.

Elevated soil salinity exerts adverse effects on plant physiological processes, encompassing growth and development. The accumulation of excessive salt in the soil disrupts cellular functions and crucial metabolic processes, including seed germination and photosynthesis, leading to physiological abnormalities and even potential death of the plant. Salt stress also detrimentally impacts various physiological traits of plants, such as respiration rates, transpiration, stomatal density, and count. Plants experience salt-related damage through two primary mechanisms: Firstly, osmotic stress, which impairs water absorption and suppresses cell growth and division; Secondly, ionic toxicity, which disrupts ionic balance and cellular processes, ultimately culminating in premature senescence [7]. Salinity-exposed plants have an abundance of Na⁺ and Cl⁻ ions in the soil, which are absorbed by the plant more quickly and subsequent depletion of other essential ions crucial for its growth and development. For example, it causes ionic stress by preventing K⁺ accumulation and upsetting the balance of nutrients in plants. When this occurs, it affects the relationship between plants and water by bringing about physiological drought conditions. This causes osmotic stress, which thus causes a deterioration in stomatal conductance (g_s) and photosynthetic enzyme activity, in turn causing plants to produce reactive oxygen species (ROS) [7]. As a cumulative result, salinity disrupts redox homeostasis, inhibiting electron transport chains’ ability to move electrons to oxygen reduction pathways in different locations of the cell, causing excess ROS in plants [8, 9].

Though the synthesis of ROS is a natural aspect of plant metabolism, their excessive accumulation can negatively interact with different components of cells like proteins, nucleic acids, lipids, and chlorophyll (Chl). Elevated ROS levels can harm the organelles, cells, and tissues of both the shoot and root systems, affecting enzymes, cell walls, and membrane functions. The role of ROS in plants swings between acting as signaling molecules and causing oxidative damage, depending on the balance between their production and removal. The equilibrium between the ROS and the antioxidant defense mechanism is disturbed by oxidative stress which is brought on by salinity.

Antioxidants are essential for neutralizing ROS and play a significant role in counteracting the stress conditions imposed by abiotic factors [10]. Generally, plants use their oxidative stress defense mechanism to delay their cell death by protecting cells from ROS-induced oxidative stress, protein degradation, lipid peroxidation, and damage to DNA and nucleic acids. This system maintains cellular integrity and enhances stress resilience in plants. To counteract the surge in ROS, plants have developed various antioxidant defense strategies against environmental stressors [11]. Recent studies primarily concentrate on physiological, biochemical, and molecular strategies to improve a plant’s resilience to salt stress by mitigating oxidative stress. Given the discussed elements, employing an external stress defense system emerges as a critical method for alleviating oxidative stress due to salinity. Furthermore, these external elicitors have been found to boost photosynthetic activity, gas exchange, photosynthetic pigments, antioxidant responses, ion balance, and hormone signaling pathways, thereby enhancing ROS metabolism and the ability to tolerate salinity in plants. This chapter offers a detailed examination and recent insights into the mechanisms and responses of various external strategies to confer salt-induced oxidative stress tolerance.

2. Overview and mechanisms of salt stress

Salt stress, particularly prevalent in coastal regions, poses a major challenge for plants. From the beginning of agriculture, 10,000 years ago, the increase in salinity in soil has been considered a major environmental issue. After soil erosion, salinity is the leading reason for global land degradation, affecting about 33% of irrigated land and 20% of cultivated land [12]. Salinization can severely inhibit cropping, reduce yields by 10–25%, and lead to desertification [13]. Due to the buildup of excessive salt, stress can halt crop growth and lead to crop death [7].

Plants respond to salt stress differently based on their resistance. Glycophytes cannot grow in high Na salt concentrations [14], whereas halophytes tolerate high salt levels [15]. Halophytes are further categorized based on their salt tolerance into severe euhalophytes and intermediate oligohalophytes [16]. Facultative halophytes thrive in non-saline environments, while obligate halophytes do not [17]. Many crop species are sensitive to salt, and their growth response to salinity varies significantly [18]. Even NaCl at lower concentrations than seawater can disrupt crop development [19]. Halobacteria are the only organisms that tolerate salt at the molecular level [20]. High levels of soluble salts affect plant development through osmotic inhibition, toxicity, and nutritional impacts mediated by specific ion effects or direct toxicity. Salinity effects can be categorized as osmotic, nutritional, and toxic, with the first two being secondary salt-induced stresses and the latter a primary salt injury [21]. Plants may defend against osmotic dehydration in secondary stress injuries by accumulating salt until the osmotic concentration exceeds that of the root medium. In contrast, primary salt injury worsens with salt accumulation.

Various physiological traits are related to a plant’s capacity to adapt and yield in highly saline conditions. For example, most halophytes are succulent, diluting internal salt concentrations [15]. Some species have salt-excreting glands, while others control turgor through organic solute synthesis or adapt by developing small leaves, water-storage hairs, and aerenchyma [15]. Salinity remains a critical challenge in global agriculture and is expected to intensify. Addressing plant salt tolerance remains complex, necessitating innovative solutions and continued research. Differences in compartmentation, ion selectivity, and water usage between halophytes and glycophytes are notable, with some plant species showing greater adaptability to salty conditions.

3. Reactive oxygen species generation and its consequence on plants under salinity

Reactive oxygen species, which act as either signaling molecules or cell-damaging agents, increase under high salinity, potentially leading to cell and plant death. Plants generate abundant amounts of ROS, including free radicals like superoxide (-O₂^•−), hydroxyl radical (^•OH), and non-radicals like hydrogen peroxide (H₂O₂) and singlet oxygen (¹O₂) [22, 23]. Additional forms are the peroxy radical (ROO^•), alkoxy radical (RO^•), excited carbonyl (RO^•), and H₂O₂ organic hydroperoxide (ROOH) [22, 24]. The balance between ROS generation and their removal regulates whether they function as stressors or signaling molecules. Oxidative stress occurs when this balance is disrupted under abiotic stress, leading to damage that is counteracted by the plant’s antioxidant protection system, comprising enzymatic and non-enzymatic components [22, 25].

Salinity induces osmotic stress within cells, quickly hindering water absorption and cell growth, causing ionic toxicity that leads to long-term ionic imbalance and cellular disruption [7]. Excessive salt reduces plant yield and can lead to death by disrupting mineral distribution and damaging cell membranes.

Higher accumulation of Na⁺ and Cl⁻ ions by greenery exposed to saline soil reduces essential ions and disrupts redox balance, leading to increased ROS production (Figure 1). This results in osmotic and ionic stresses, affecting g_s and photosynthetic activity [7]. Studies show that salinization increases malondialdehyde (MDA) and H₂O₂ levels, causing more damage to the root than the shoot due to direct exposure to saline conditions [26, 27]. In sorghum, salt stress led to higher MDA levels in roots along with increased H₂O₂ in shoots [28]. Salinity also influences plant development by affecting gene expression related to ROS metabolism and interacting with stress-related pathways, although the exact mechanisms remain under study [29].

Figure 1.

Oxidative stress and antioxidant defense in plants under salinity. This illustration shows that a balance between ROS and antioxidant defense is necessary for plant survival under salt stress [22].

Cell organelles for instance cell walls, plasma membranes, chloroplasts, mitochondria, peroxisomes, endoplasmic reticulum, glyoxysomes, cytosol, and apoplast produce ROS through various pathways [24, 30]. Stress conditions lead to increased formation of rigid cell walls, as peroxidase (POD) and ROS polymerize phenolic compounds and glycoproteins. Malate dehydrogenase from nicotinamide adenine dinucleotide (NADH) takes part in catalyzing the formation of H₂O₂ [31].

The plasma membrane produces a significant amount of O₂^•− due to the action of nicotinamide adenine dinucleotide phosphate (NADPH) reconciled by quinone reductase and NADPH oxidase. With the latter, an electron is transferred to create O₂^•− out of cytoplasmic NADPH. This reactive radical is later transformed into H₂O₂ [32]. Chloroplasts are crucial organelles for ROS production, especially under reduced g_s and CO₂ assimilation rates. Excited triplet chlorophyll (3Chl*) accelerates photo-oxidation, leading to overproduction of ROS and hindrance of the photosynthetic electron transport chain (ETC) [33, 34]. Photosystems I and II (PS I and PS II) are sites within the chloroplast where singlet oxygen (¹O₂) and O₂^•− are abundantly generated [23].

In non-green plant components, mitochondria are primary sites for ROS formation, with ubiquinone (complex I) and the ETC (complex III) being common sources of O₂^•−. Superoxide dismutase (SOD) viz. Mn-SOD and Cu-Zn-SOD induced the transfiguration of O₂^•− into H₂O₂ [34, 35]. Peroxisomes are believed to primarily produce ROS through glycolate oxidase (GOX), leading to stomatal closure and reduced CO₂ availability for RuBisCO, thereby causing photorespiration and H₂O₂ production [36, 37].

In the endoplasmic reticulum, reduced NADPH levels lead to activities by cytochrome P450 and cytochrome P540 reductase, resulting in minor production of O₂^•− [38]. Glyoxysomes, derived from peroxisomes, engage in fatty acid β-oxidation and the glyoxylate cycle, where GOX along with urate oxidase activities, produce both O₂^•− and H₂O₂ [39].

In the cytosol, the degree of ROS formation is lower than in other compartments. However, the cytosol plays a vital participation in redox signaling and ROS generation, influencing gene expression in the cell nucleus [40]. Quinone reductase, NADPH oxidase, and lipoxygenases (LOX) are key enzymes contributing to ROS production in apoplasts [41, 42].

Excessive production of ROS damages proteins, lipids, carbohydrates, and DNA, leading to nucleic acid damage. Under stress, oxidative bursts damage cell lipid membranes and cause lipid peroxidation, targeting the unsaturated C-C double bonds in membrane phospholipids (Figure 2). The phases of lipid peroxidation include initiation, propagation/progression, and termination, with MDA serving as a marker for oxidative damage [25, 43, 44].

Figure 2.

Cellular impairment caused by reactive oxygen species and its consequences in plants under salinity. Salt stress causes overgeneration of ROS, which leads to damage to lipids, proteins, DNA, and carbohydrates. Various damage subsequently results in cell death and reduction of plant growth and yield reduction [43].

Protein oxidation is the process of chemically modifying proteins either by ROS directly or by attaching them to breakdown products of fatty acid peroxidation [45]. Several ROS selectively cause protein denaturation, among which the ^•OH is notably aggressive, indiscriminately damaging protein molecules [22]. Non-radical oxidants typically cause less damage due to their slower oxidation rates, whereas rapid radicals significantly damage the protein structure, mainly by extracting hydrogen atoms from the α-carbon, resulting in stabilized carbon-centered radicals. This damage alters protein function through degradation of the peptide backbone, leading to alterations such as glutathionylation, carbonylation, nitrosylation, and disulfide bond generation.

Among free radicals, ^•OH is particularly harmful as it oxidizes sugar residues, alters nucleotide bases (purine and pyrimidine), and induces DNA strand breaks, facilitating cross-linking between DNA and proteins [44]. In contrast, H₂O₂ and O₂^•– do not typically engage with nucleotide bases, while ¹O₂ primarily responds to guanine [25]. Hydroxyl radicals also contribute to DNA damage by removing hydrogen from the C−H bonds of 2-deoxyribose and methyl groups, leading to the formation of deoxyribose radicals, hydroxymethyl urea, and thymine glycol. This can result in the oxidation of nucleotide bases, forming damaging compounds such as 8-hydroxyquinine and dehydro-2-deoxyguanosine, potentially leading to plant destruction [44].

In plants, the first pathways affected by free radical damage are the tricarboxylic acid (TCA) cycle and glycolysis. For instance, oxidative stress gives rise to the discontinuation of key enzymes in the pentose phosphate pathway, such as glyceraldehyde 3-phosphate dehydrogenase and fructose-1,6-bisphosphate aldolase, resulting in increased levels of cycle metabolites like ribose 5-phosphate and ribulose 5-phosphate. These changes facilitate NADPH synthesis and accelerate carbon flow to counterbalance ROS levels [22, 46]. Additionally, oxidative stress restricts the action of aconitase in the TCA cycle, leading to increased citrate biosynthesis, and impacts plant health by decreasing glycolysis, TCA cycle metabolism, and amino acid transport [46].

Salinity directly induces ionic and osmotic stress as well as secondary stresses including ROS-induced oxidative damage. At a certain low concentration that varies based on several conditions, these ROS perform a signaling role. However, the increased formation of ROS alters the equilibrium between ROS buildup and removal, leading to the destruction of various biomolecules in response to varied environmental stresses. In extreme cases, this damage to biomolecules includes the destruction of nucleic acids, protein oxidation, lipid peroxidation, enzyme deactivation, and Chl deterioration [25].

Young and mature leaves are the least impacted by salt stress, whereas root tissues suffer the most. A dose-dependent reduction was noted in root-shoot length, stem diameter, and plant biomass including root and shoot dry weight. The photosynthetic pigments Chl a, Chl b, Chl (a + b), Chl a/b ratio, and carotenoid (Car) content were reduced in salt stress. Due to salt exposure, the degree of Na⁺ increased, and K⁺ decreased; ultimately, the Na⁺/K⁺ ratio increased. On the other hand, Ca²⁺ content is reduced in a dose-dependent manner. Physiological attributes like relative water content showed a declining trend, and proline (Pro) content was uplifted because of salt accumulation [47].

In our experiment, we used soybean (Glycine max) plants to induce oxidative stress tolerance to salt, which was later alleviated by Bacillus subtilis (Figure 3). Oxidative stress indicators MDA and H₂O₂ were elevated for ROS generation. For analyzing the production of ROS (H₂O₂ and O₂^•–) spot localization using staining (using diaminobenzene and nitroblue tetrazolium) was carried out. All of the salt treatments showed notable alterations. The brown H₂O₂ area and the dark blue O₂^•– areas were more noticeable in comparison to the control as the salt concentration increased [47].

Figure 3.

Localization of the spots of H₂O₂ (A) and O₂^•− radicals (B) on the leaves of soybean as affected by bacillus sp. in response to different concentrations of stress. Here, C, BP, and BS indicate the control, seed inoculation, and soil with B. subtilis, respectively [47].

In the ascorbate-glutathione (AsA-GSH) pool, AsA and GSH content was lessened, whereas dehydroascorbate (DHA) and oxidized glutathione (GSSG) level was escalated, which ultimately alleviated the ratio of AsA/DHA and GSH/GSSG. In the case of enzymatic antioxidants, ascorbate peroxidase (APX), glutathione reductase (GR), POD, glutathione S-transferase (GST), and glutathione peroxidase (GPX) exhibited elevation on the contrary monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), SOD, and catalase (CAT) contents were scaled down under the salt exposure at different doses. The reduction was unveiled in glyoxalase I (Gly I) and Gly II contrarily methylglyoxal (MG), which indicated an increasing trend [47].

4. Approaches to mitigate ROS toxicity in plants under salinity

In order to protect themselves from oxidative stress, plants need an efficient antioxidant defense mechanism consisting of non-enzymatic (such as AsA, GSH, α-tocopherol, non-protein amino acids, phenolic compounds, alkaloids, carotenoids, and flavonoids), and enzymatic (such as SOD, POD, APX, CAT, MDHAR, DHAR, GR, GST, and GPX) antioxidants [43]. Researchers found various ways to enhance antioxidant defense in pants to protect them from oxidative stress caused by salt.

4.1 Exogenous application of chemical substances

Chemical substances applied exogenously, through priming, irrigation, soil addition, or foliar spraying in small amounts, can mitigate ROS-induced oxidative damage under salt stress (Table 1). Abiotic stress tolerance, like salinity tolerance, can be enhanced by these chemicals by boosting the antioxidant defense mechanism and reducing oxidative damage at the cellular level [59].

Species	Dose of NaCl	Chemical substances and dose	Method of application	Major effects	References
Triticum aestivum	NaCl (75, 150 and 225 mM)	Trehalose (10 mM)	Seed priming	Reduced lipid peroxidation and H2O2 content; reduced Pro accumulation and soluble sugar content	[48]
Solanum lycopersicum	NaCl (150 mM)	Melatonin (150 μM)	Added to nutrient solution	Reduced O2^•− and H2O2 generation; increased Chl content; promoted APX, MDHAR, DHAR, GR, CAT, APX, SOD, and POD activities	[49]
S. lycopersicum	NaCl (100 mM)	Spermine (50 and 100 μM)	Foliar application	Decreased O2^•− and H2O2 content, lipid peroxidation, and EL; increased Pro, soluble sugar, GB content; enhanced AsA-GSH cycle enzymes, SOD, and CAT activities	[50]
Capsicum annuum	NaCl (2000 and 4000 ppm)	Salicylic acid (1 mM) and Pro (10 mM)	Foliar application	Enhanced Chl a and b content, leaf RWC; decreased O2^•− and H2O2 contents and lipid peroxidation; decreased CAT and POX activities	[51]
Cucumis sativus	NaCl (50 mM)	Sodium silicate (0.3 mM)	Added to nutrient solution	Decreased O2^•− and H2O2 content; promoted Pro, SA, IAA content, and decreased ABA content	[52]
Luffa acutangula	NaCl (100 mM)	Putrescine (100 μM) and kinetin (100 μM)	Foliar application	Reduced O2^•− and H2O2 content, lipid peroxidation, EL; promoted the activities of APX, SOD, CAT, and GR	[53]
Oryza sativa	NaCl (150 mM)	Melatonin (50, 100, 150 and 200 μM)	Foliar application	Enhanced the Na^+ efflux and K^+ influx, decreased H2O2 content	[54]
Phaseolus vulgaris	NaCl (50 and 100 mM)	Glycine betaine (25 and 50 mM)	Foliar application	Reduced MDA content, EL, and Na^+ accumulation; increased the synthesis of Chl and upregulation of SOD, POD, and CAT activities	[55]
Helianthus annus	NaCl (120 mM)	α-tocopherol (100, 200, and 300 mg L^−1)	Seed priming	Reduced H2O2 and EL; enhanced AsA and total phenolics content; upregulated the activities of SOD, CAT, POD, and GR	[56]
O. sativa	NaCl (150 mM)	Spermidine (0.5, 1 and 1.5 mM)	Seed priming	Declined O2^•− generation, lipid peroxidation, and EL	[57]
O. sativa	NaCl (50 mM)	Thiourea (7.5 μM) and H2O2 (1 μM)	Foliar application	Promoted the activities of antioxidant enzymes like SOD, CAT, APX, and GR	[58]

Table 1.

Exogenous application of different chemical substances to mitigate ROS toxicity under NaCl-induced salinity.

4.1.1 Amino acids and their derivatives

The external application of various amino acids has emerged as a promising strategy to counteract ROS toxicity caused by salinity. Proline (Pro) is noteworthy as it acts as a molecular chaperone because of its ability to forage ROS and maintain cellular redox balance [60]. In a saline media where maize seedlings were grown, the addition of Pro and glycine betaine (GB) separately led to enhanced antioxidant systems and osmolyte metabolism, significantly reducing the generation of O₂^•− and H₂O₂. Furthermore, Pro and GB applications also bolstered the AsA-GSH pool and the glyoxalase system, providing cellular protection against excessive ROS, MG, and other toxic metabolites [61]. Wani et al. [62] demonstrated that spraying 20 mM Pro on Brassica juncea under varying salt concentrations (78, 117, and 176 mM NaCl) boosted endogenous Pro levels and the actions of antioxidant enzymes like CAT, POD, and SOD. Application of GB (25 and 50 mM) on Phaseolus vulgaris at the vegetative and flowering stages under salt stress improved shoot K⁺ content, lessened Na⁺ buildup, and enhanced the K⁺/Na⁺ ratio. This treatment also increased Pro and GSH levels, contributing to effective ROS scavenging and a noticeable reduction in oxidative stress [55]. Treating Glycine max plants with cysteine, a thiol-group containing α-amino acid, counteracted salinity effects through Pro accumulation and decreased H₂O₂ and lipid peroxidation levels, alongside increased action of SOD and CAT [63]. The addition of γ-aminobutyric acid along with salt to the nutrient solution reduced Na⁺ uptake in Solanum lycopersicum and mitigated the excessive accumulation of O₂^•− and H₂O₂ [64]. Exogenous melatonin (150 μM) protected the photosystem by enhancing antioxidant enzymes and the AsA-GSH pool, aiding in the detoxification of ROS caused by salinity [49]. Additionally, melatonin application reduced the root Na⁺/K⁺ ratio under stress induced by salinity, aiding in maintaining ion homeostasis [54]. Pre-treating young B. napus seedlings with exogenous β-aminobutyric acid (BABA, 150 μM) for 48 h before exposing them to salt environments (100 and 150 mM NaCl) for another 48 h showed higher tolerance to salt stress by upregulating antioxidants to neutralize toxic ROS [65].

4.1.2 Phytohormones

Exogenously applied plant growth regulators, including indole-3-acetic acid (IAA), jasmonic acid (JA), salicylic acid (SA), silicon (Si), gibberellic acid (GA), cytokinin (CK), and brassinosteroids, is a cost-effective method to alleviate the harmful consequences of abiotic stresses such as salinity. The combined application of kinetin (10 μM) and 24-epibrassinolide (EBL, 1 μM) has been shown to enhance photoprotection under salinity conditions (100 mM NaCl) by improving tissue water potential, mineral assimilation, Na⁺ ion restriction, metabolite accumulation, and the antioxidant system. This is evidenced by reductions in H₂O₂ content, lipid peroxidation, and activities of protease and LOX, indicating ROS detoxification in kinetin and EBL-treated plants [66].

Raju et al. [67] showed that supplementation individually with IAA (10⁻⁵ M) or in combination with 28-homobrassinolide (10–8 M) reduced Na⁺ buildup in the roots and shoots of S. melongena under various concentrations of NaCl (5 and 15 mM). Additionally, applications of IAA and 28-homobrassinolide improved the efficiency of PS II and the metabolism of nitrogen. A decrease in O₂^•− and H₂O₂ levels due to enhanced antioxidant activity such as increased SOD, CAT, POD, and GST was observed, highlighting the positive effects of IAA and homobrassinolide.

Combined seed priming and foliar spraying of JA (60 μM) increased salt stress (100 mM NaCl) tolerance by boosting the endogenous levels of GA, JA, and abscisic acid (ABA). Exogenous application of JA under salt stress modified physiological processes like the rate of photosynthesis, transpiration, and intercellular concentration of CO₂, significantly reducing H₂O₂ and lipid peroxidation in both salt-sensitive and tolerant cultivars of G. max [68].

In S. lycopersicum, seed priming and simultaneous application of SA (10 μM) mitigated salinity-induced ion toxicity and osmotic stress (125 mM NaCl). Exogenous SA application was found to elevate the endogenous SA level, inducing salt tolerance through the stimulation of the endogenous hormone signaling pathways [69]. Salicylic acid application (0.75 mM) under 125 mM NaCl salinity stress significantly activated antioxidant enzymes like CAT (by 2.25-fold), APX (by 2.22-fold), and SOD (by 1.76-fold), leading to reduced H₂O₂ accumulation and protection against peroxidation of lipid and leakage of electrolyte [70].

Silicon (SiO₂) application also ameliorated various physiological and biochemical attributes, safeguarding plants from the adverse consequence of salt stress by downregulating genes associated with ROS and reactive nitrogen species and enhancing antioxidants, both enzymatic and non-enzymatic [71]. Pre-treating seeds with EBL (10⁻¹ M) improved leaf relative water content (RWC), Pro, GB, and flavonoid levels in S. lycopersicum seedlings under NaCl stress, reducing ROS toxicity alongside upregulated actions of antioxidants [72].

4.2 Application of organic amendments

Organic amendments like biochar (BC), lignite, and compost have been shown to lessen the damaging effects of oxidative stress by regulating the synthesis of plant enzymes endowed with antioxidant properties. Under stress induced by salinity, adding compost to soil increases the ratio of K⁺/Na⁺ in S. lycopersicum seedlings. Additionally, the upregulation of enzymes connected to the AsA-GSH cycle and activities of other enzymatic antioxidants was observed in compost-treated, salinity-stressed plants [73]. Biochar employment in saline soils has been shown to enhance soil physicochemical properties, including increases in organic matter content and cation exchange capacity, along with a decrease in exchangeable Na ions. In salinity stress, the beneficial effects of BC were highlighted by Farhangi-Abriz and Torabian [74], who stated that it reduced O₂^•−, H₂O₂ content, and lipid peroxidation in P. vulgaris, leading to decreased action of CAT, APX, SOD, polyphenol oxidase (PPO), and POD, and also reduced concentrations of osmolytes like Pro, GB, and soluble sugar. Furthermore, Torabian et al. [75] demonstrated that the growth of Vigna radiata under control and salt stress improved with BC and lignite applications at 50 and 100 g kg⁻¹ soil, attributed to the enhancement of potassium (K), calcium (Ca), magnesium (Mg), iron (Fe), and zinc (Zn) and diminution of Na and ROS production. In saline soil, compost supplementation improved endurance of salt stress in Chenopodium quinoa by improving actions of SOD, CAT, and APX, particularly at the time of foliar spraying of plants with Pro (0.5 and 1 mM) and/or trehalose (2.5 and 5 mM; [76]). Additionally, polysaccharide-enriched seaweed liquid extract, used as a biostimulant or biofertilizer, was seen to reduce salinity-induced ROS toxicity in plants. Hashem et al. [77] reported the beneficial effects of three seaweeds on B. napus, by documenting increased growth and yield attributes, such as higher total Chl content, total carbohydrate accumulation, and enhanced endogenous phytohormone levels (IAA, GB, GA, and CK) when grown in seaweed-incorporated soil under normal or salinity stress conditions (75 and 150 mM NaCl).

4.3 Use of microorganisms

4.3.1 Plant growth-promoting rhizobacteria

The restoration of soil health heavily relies on microbial communities in soil [78]. These microbial communities can be adjusted to improve the rejuvenation of agricultural lands that have been degraded due to different types of abiotic imbalances, especially salinity problems. It is essential to comprehend the role of beneficial microbes to maximize soil restoration endeavors, with an emphasis on groups such as rhizobacteria and mycorrhizal fungi that promote plant growth and development. The utilization of plant growth-promoting rhizobacteria (PGPR) emerges as a productive tactic for mitigating the adverse consequences of salinity stress on plant vitality [79, 80, 81]. These bacteria thriving in the rhizosphere promote plant health through various mechanisms, including hormonal stimulation, siderophore synthesis, exopolysaccharides secretion, osmoprotectant accumulation, ion exchange, and the stimulation of antioxidant enzymes (Figure 4) [82]. Improved antioxidant system by PGPR plays a critical role in detoxifying ROS molecules in plants to deal with ROS-induced oxidative stress [83]. Plant growth-promoting rhizobacteria can decrease the stress-induced activities of ROS in plants via two mechanisms: The generation of antioxidant molecules and the alteration of gene expression of plants that synthesize ROS scavengers. For example, administering halotolerant Enterobacter sp. UPMR18 to Abelmoschus esculentus plants resulted in a notable augmentation of antioxidant enzymes, including CAT and SOD, within the treated plants [84]. Research findings indicate that certain microorganisms, including Bacillus licheniformis and Pseudomonas plecoglossicida, which have the capability to form biofilms, may positively influence the growth of Helianthus Annuus when subjected to salt stress. This influence is attributed to their ability to increase the production of 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase, phytohormones, and a variety of antioxidant enzymes, such as CAT, SOD, and GPX [85]. In a separate study, a notable reduction in H₂O₂ content within plant nodules was observed in Vigna unguiculata when seeds were simultaneously inoculated with Bradyrhizobium and PGPR (either Actinomadura sp. or Paenibacillus graminis). This reduction is attributed to changes in the collective amounts of reduced and oxidized forms of AsA and GSH, coupled with increased SOD and CAT activities. Specifically, plants subjected to coinoculation with Bradyrhizobium and Streptomyces sp. exhibited a 55% increase in CAT activity compared to plants inoculated with Bradyrhizobium alone [86]. Similarly, Yasmin et al. [87] reported that rhizobacteria belonging to Pseudomonas sp. and Bacillus sp. enhanced salt tolerance in G. max L. by adjusting the concentrations of MDA, CAT, PPO, SOD, POD, APX, and Phenylalanine ammonia-lyase (PAL) within plant system. The advantageous impacts of Rhodopseudomonas palustris G5 in improving salt stress resistance in Cucumis sativus were demonstrated through increased levels of phytohormones and soluble sugars alongside elevated activities of SOD and POD enzymes. Strain G5 is capable of fixing nitrogen and solubilizing K and P [88]. Additionally, in a separate experiment, the combination of bacterial inoculation (Pseudomonas sp. RS-198 and Azospirillum brasilense RS-SP7) and treatments with phytohormones including SA and JA were employed to alleviate the detrimental consequences of salt stress caused by 50 and 100 mM NaCl in Brassica napus. Results indicated that the simultaneous application of Pseudomonas and SA yielded the most favorable outcome, reducing the generation of O₂^•−, H₂O₂, and lipid peroxidation by increasing endogenous SA levels and antioxidant enzyme activities [89].

Figure 4.

Plant growth-promoting bacteria and rhizospheric fungi induce the production of antioxidant enzymes and induce their gene expressions in plants related to salt stress and antioxidant enzymes when exposed to saline conditions, thereby mitigating the stress.

Furthermore, El-Esawi and coworkers [90] revealed that introducing Bacillus firmus SW5 into soybean plants enhanced the activation of genes linked to salinity tolerance and antioxidant enzymes (APX, SOD, POD, and CAT) particularly while exposed to high salt concentrations (80 mM NaCl). Additionally, PGPB-mediated upregulation of genes such as GmFLD19 and GmNARK has been found to alleviate oxidative stress in soybeans, leading to reduced Na⁺ and MDA and enhanced effectiveness of antioxidant enzymes in plants [80]. Moreover, the synergistic action of Piriformospora indica and Azotobacter chroococcum exhibited the ability to promote the growth of Artemisia annua L. by easing MDA content and fostering the levels of antioxidants [91]. These findings underscore the significant role of potential PGPR in alleviating ROS in plants subjected to salinity stress, wherein the heightened levels of PGPR-induced antioxidants contribute to enhanced growth and yield to mitigate the stress.

4.3.2 Rhizospheric fungi

The judicious application of arbuscular mycorrhizal fungi (AMF) has been shown to improve various physiological and biochemical characteristics of crop plants facing different types of abiotic stresses, including salinity (Figure 4). When subjected to salt stress, AMF can bolster the development and productivity of plants by boosting water and nutrient absorption, preserving ion balance, mitigating ROS toxicity, controlling lipid peroxidation, and accumulating osmolytes in inoculated plants [92]. The symbiotic interactions between plants and AMF also augment the synthesis of SA, JA, and other inorganic nutrients. It has been observed that under salt stress conditions, AMF-treated Cucumis sativus exhibited higher levels of Ca, N, Mg, K, and P compared to non-inoculated plants [93]. Furthermore, mycorrhizal treatment in Lactuca sativa has led to increased Pro accumulation, enhanced N uptake, and reduced Na⁺ accumulation in contrast to plants without mycorrhizal treatment under saline conditions [94]. Although one of the most important anticipated facets of this symbiosis is the stimulation of the antioxidant activities in plants, investigations into the role of AMF in amplifying antioxidant activity in plants under saline stress have yielded conflicting results. Some studies indicate amplified action of antioxidant enzymes, like SOD, CAT, POD, and APX [95], while others report nonsignificant changes or reduced activity. For instance, tomato plants inoculated with mycorrhizae exposed to salinity stress exhibited varying responses in the activation or involvement of these ROS scavengers [96, 97].

5. Conclusion

Environmental sustainability is disrupted by climate change, primarily driven by global warming. This results in weather fluctuations that negatively impact agricultural practices and, hereafter, production declines. Salinity is one of the major destructive environmental factors affecting agriculture, which is exacerbated by climate change. Intensification of salt in the soil creates this stress condition, disrupting cellular functions and metabolic processes and leading to plant death. Salt stress exacerbates plant damage through increased osmotic stress and ionic toxicity. Affected plants exhibit an abundance of Na⁺ and Cl⁻ ions, which are absorbed more rapidly than vital ions, leading to physiological drought conditions and osmotic stress, ultimately originating ROS, resulting in membrane damage and metabolic abnormalities. In this regard, various antioxidants, phytohormones, signaling molecules, and plant nutrients have been identified as crucial for the detoxification of ROS in situations of abiotic stress, in turn enhancing the plant’s defense system. Different approaches have been taken under consideration to lessen this adversity, including the exogenous application of amino acids, polyamines, vitamins, plant growth-promoting substances, organic amendments, and exploiting the microorganisms that are beneficial for plants, as well as genetic approaches to scavenge ROS and improve plant physiological and metabolic functions. These interventions offer a significant opportunity for both soil and plants to alleviate salt stress, particularly in coastal regions where salinity is a major concern.

Acknowledgments

We acknowledge Naznin Ahmed for her help in collecting some important literature and critical reading of the manuscript.

Conflict of interest

The authors declare no conflict of interest.