Salinity Stress in Plants: Challenges in View of Physiological Aspects

Abstract

Increasing the worldwide population, the food supply has become a global crisis due to the existence of various environmental stresses. Salinity after drought is one of the devastating environmental stresses that affects about 50% of the world’s agricultural lands. It is considered as one of the important abiotic stresses that cause plant growth restriction in different stages such as seed germination, photosynthesis, hormonal regulation, nutrient uptake, and seed quality and quantity. Under salinity conditions, plants undergo numerous changes as morphological (early flowering, prevention of lateral shoot development, and root adaptations), physiological (Na+/K+ discrimination, osmotic adjustment, ion homeostasis, and stomatal responses), and biochemical (accumulation of polyamines, antioxidant activity, proline, and change the hormone level). With the ever-increasing expansion of saline lands and highly costs spending for their rehabilitation, the preparation of high-yielding lines/genotypes tolerant to salinity will be of particular importance. Being aware of various pathways involved in plant resistance to salinity stress can be an effective tool to increase crop production and cultivated area in different parts of the world.

1. Introduction

Abiotic stress is one of the dreadful environmental stresses that affect plant growth and crop yield, even in irrigated areas throughout the world. Salinity stress is one of the major abiotic stresses that limits crop production and agricultural sustainability in many areas of the world because of the increased use of low-quality water for irrigation. An important issue for agricultural science and food production in the world is the study of salt stress mechanisms in crops. The plant response to high NaCl concentrations is complex and comprehensive; it contains numerous processes that should be correctly coordinated. The extra salt concentrations affect plants, leading to ionic imbalance and osmotic stress because of the accumulation of ions like Na⁺ and Cl⁻. Moreover, salt stress leads to mineral homeostasis of K⁺ and Ca²⁺. Recently, a new gene family involved in salt stress response in crops has been reported based on achievements in genomics, molecular biology, and transcriptomic procedures [1].

Soil salinity is considered as a destructive environmental factor that has severe negative effects on seed germination, crop growth, and productivity [2]. Of the 230 million hectares of farmland in use around the world, 20% is affected by salt followed by their increase annually as a result of various factors including (1) inappropriate crop irrigation practices, (2) excessive fertilization and plowing, and (3) natural phenomena such as salt intrusion into coastal zones resulting from rising sea levels [3, 4]. For instance, around 100 million hectares of farmland in China suffer salinity stress [5]. In arid and semi-arid regions, salinity is becoming a more and more dreadful threat due to limited rainfall, high evapotranspiration, and extreme temperatures coupled with poor water and soil management [6, 7]. Globally, salinity is an important stress that affects a large proportion of crop productivity and agricultural soil [8]. Since, demand for food production is growing by enhancing world population, making use of salty lands to compensate for food shortages is of great importance [9]. Thus, scientists are attempting to increase food production by 70% to avoid the risk of food shortages for 9.3 billion people by 2050 [10].

The fact that the continuously growing population and meeting its demand has attracted agricultural politicians to focus on crop productivity enhancement. In this route, environmental stresses could be recognized as major obstacles to crop production [11]. Among all abiotic constraints, salinity stress is one of the major limitations for crop production, which leads to ionic imbalances, osmotic stress, and secondary stresses for glycophytes [12]. Currently, climate change and environmental stresses negatively influence arable lands due to irrigation malpractices, which results in the accumulation of sodium chloride (NaCl) in soil [13]. Besides inaccurate cultivation practices, arable lands may confront some natural phenomena including salty water on the coasts and contamination resulting from parent rock and oceanic salts, which threaten the productivity of arable land under cultivation. Although Na⁺ causes toxicity in soil under salinity conditions, Cl⁻ anion can play an important role in causing some plant species to be sensitive [14].

Salinity has a negative effect on growth and development processes in plants, followed by their seed/biomass yield [15]. Salt stress negatively influences plant growth by germination reduction, decrease of aerial organ growth and dry matter production, as well as disturbance of nutritional imbalances, the complex interaction of hormones, osmotic adjustment, and specific ion toxicity [16, 17]. Increasing salinity decreases the leaf area, followed by hindering leaf development and a decrease in light absorption and photosynthesis rate [18]. If the new leaves appear, they may be weak and show burning symptoms when they turn to mature. In total, there is a positive correlation between leaf number/leaf area and photosynthetic rate, which means the less leaf number/area, the less photosynthetic rate following the decline of dry weight matter [19, 20]. Salinity disturbs ions transport in different plant’s organs, which causes a decline in vegetative and reproductive quality.

Potassium is an essential nutrient for plant growth, which plays the main role in creation of osmotic pressure and protein production of cells [21, 22]. Salinity (sodium chloride) interferes with the active absorption of this element, since it prevents the selective absorption of cells. Besides, the competition of sodium with potassium in cells brings about a decrease in inactive absorption of potassium due to more abundance of sodium than potassium (Figure 1) [23, 24].

Figure 1.

A general sight of physiological, biochemical, and morphological effects of salt stress in plants.

Since crops play an important role in the economy of agricultural societies and salt stress has strong and diverse effects on overall crop growth, the objective of this chapter is to accurately detect and awareness of the biological processes involved in salinity stress to prevent severe damage in consideration of various aspects of morphological, physiological, and biochemical mechanisms. In addition, the introduction of salt-tolerant cultivars could be the other management strategy that leads to decreased damages resulting from salt stress.

2. Influence of salt stress

About 50% of agronomical lands are affected by different ranges of salt stress worldwide [25]. Among different climatic areas, it should be noted that arid and semi-arid zones are extremely sensitive to salt stress, which means salinity is considered the most significant obstacle to agronomical and horticultural production. Salt leads to decreased plant growth in two ways in both soil and water. In one way, the existence of salt in soil solution declines plants’ capability in relation to water absorption, which is known as an osmotic effect or water shortage. In another way, extra salt entrance by transpiration results in damage to leaf cells [26].

Most morphological traits in plants such as leaf area, biomass, seed weight, root system, plant height, spikelet per panicle, and tillers per plant reduce under high salt concentration, leading to a reduction in grain yield and harvest index [27, 28]. Salt stress affects physiological and biochemical processes in plants at all developmental stages, from germination to senescence [29]. Salt stress has both osmotic and ionic or ion-toxicity effects on plants, ultimately causing oxidative stress and nutrient depletion in plant cells [30]. Continuous salt stress reduces plant cell turgor pressure, which in turn reduces cell growth; therefore, plants must osmotically adjust to maintain cell expansion and growth [30, 31, 32]. Osmotic stress (caused by the lower water potential of the external solution) is rapidly sensed by plants soon after exposure to saline conditions and leads to plant water and solute deficits [9, 33]. Osmotic stress also results in rapid stomatal closure, which reduces the plant’s ability to assimilate CO₂ and inhibits photosynthesis [34]. Aging and death of plants are caused by the accumulation of sodium (Na⁺) and chlorine (Cl) in plant cells due to ionic stress [35]. The most common explanation for Na⁺ toxicity is that it has an inhibitory effect on enzyme activities, affecting metabolism negatively, including the Calvin cycle and other pathways [36, 37]. Excess sodium in the cytoplasm also interferes with the uptake and transport of potassium and other macro and micronutrients, including nitrogen, phosphorus, potassium, calcium, and zinc [38]. Various stresses, such as osmotic stress and salinity, damage the cells and vital molecules in plant cells due to the accumulation of reactive oxygen species [23]. Under salinity tension, plants should regulate biochemical and physiological pathways related to the regulation of osmotic and ionic homeostasis, nutrient balance, and oxidative stress [39].

The continuous transfer of salt into leaves during a long period will eventually lead to high sodium and chlorine accumulation, which causes devastating effects on old leaves, since the death rate of leaves is necessary for plant survival [40]. If the newly created leaves are more than dead leaves, the plant has enough photosynthesizing leaves to produce flowers and seeds, no matter how many of them have been decreased. However, if there are more dead leaves than produced leaves, then plants cannot survive to produce seeds [41].

The plant growth response to salinity stress includes two-phase reactions over time. The first stage of growth reduction, known as “initial growth decrease” or “early phase,” is due to the osmotic effect of salt outside the root zone appearing quickly. Then, the second reduction stage, “late phase or ionic phase,” occurs, which comes from internal damage and continues for a longer period of time. What creates a differentiation between salt-sensitive plants and salt-tolerant plants is the inability to prevent salt from reaching toxic levels in transpiration leaves over time [21].

In most crops, the critical growth stage is seed germination, which exhibits toxic effects on seed embryo water uptake inhibition under salinity. However, legumes, seedlings, and developmental stages are more sensitive than the germination stage. It is observed that salinity results in limitations such as a decrease in the water potential of tissue, photosynthesis, and different stages of growth. For example, the stomatal closure caused by less availability of water to cells brings about less photosynthesis and growth in soybeans under salinity stress [42]. In another study, it was found that the early stages of growth and development in lentils are sensitive to salt stress [43].

Ionic imbalance is the other indicator of salinity conditions that cause disturbance in competitive nutrient uptake, accumulation, and transport in plants. Indeed, the concentrations of cations including Ca²⁺, K⁺, and Mg²⁺ which are vital for photosynthetic activity, decrease by different levels of salt [44]. For instance, the survey of the Na⁺/K⁺ ratio in Lotus creticus showed Na⁺ contents increase in aerial and root organs under salinity stress [45]. Moreover, the competitive uptake of Na⁺ and K⁺ ion flux caused an astonishing reduction of the Na⁺/K⁺ ratio in mungbean and chickpea, indicating a significant decrease in K⁺ and yield [46]. In legumes, it was demonstrated that different species had various responses to saline conditions, since it was determined that soybean, mungbean, cowpea, and common bean indicated salt sensitivity as Na⁺ toxicity, Cl⁻ toxicity, Na^+, and Cl⁻ toxicity, respectively [47]. Lopez-Aguilar et al. reported that the uptake and transport of Ca²⁺ and Mg²⁺ were significantly lower in cowpea and frijollilo plants under salt stress; however, these rates in Tepary bean plants showed no significant response to salinity treatments [48]. It was reported that the Na⁺/K⁺ ratio increased in the roots and shoots of Cheongcheong and IR28 cultivars of rice under salinity stress [49]. In addition, it was found that there was a significant correlation between grain dry matter and the K⁺/Na⁺ ratio under salt stress in wheat, which had an effect on the grain filling rate and its duration [21].

3. Different mechanisms of tolerance to salt stress

Plants show different salinity tolerance reactions, which are reflected in their different growth responses. To increment crop yield under salt stress, it is of great importance to recognize tolerance mechanisms consisting of ion homeostasis, compatible solute accumulation and osmotic protection, antioxidant regulation, and hormonal regulation.

The salt tolerance mechanisms in plants are divided into three groups: osmotic stress tolerance, Na⁺ expulsion from leaf, and tissue tolerance [50]. With respect to osmotic stress tolerance, this type of stress decreases cell development on the tips of roots and young leaves. A decrease in response to osmotic stress leads to an increase in leaf growth and stomata conduction, while the increment of leaf area would be profitable for plants whose soil has enough water availability. The second group is related to repulsing Na⁺ from leaves, which is assured that Na⁺ ions with toxic concentration do not accumulate within leaves, since the deficiency of excretion of Na⁺ toxic effects causes premature death of older leaves. The third mechanism is tissue tolerance, which appears to be tolerant of some tissues to Na⁺ and Cl⁻ accumulation [51].

4. Salt tolerance strategies

Salt tolerance mechanisms include processes that allow plants to resist stress, take up nutrients from the soil, and complete their life cycle under high salt concentrations in the soil. Plants that are able to grow on higher levels of salt in the rhizosphere are termed as halophytes. To enhance salt tolerance, the following strategies will be briefly reviewed, aiming at crop salt tolerance under saline conditions.

In general, the physiological responses of plants to salinity stress are divided into two main phases. The first phase is ion-independent growth reduction. It occurs within a few minutes to a few days, resulting in closing stomata and cell expansion inhibition [52]. A second phase, which pertains to the build-up of cytotoxic ion levels, happens for a relatively long period, resulting in slowing down metabolic processes, reducing leaf water potential, premature senescence, and ultimately cell death [53, 54].

4.1 Ion homeostasis and its detention in tissue

Under salt stress, plants apply an ion homeostasis mechanism to maintain a high concentration of K⁺ and a low concentration of Na⁺ in the cytosol [55]. Ion homeostasis is enough for normal growth and a necessary process for growth during salt stress [56]. Regardless of the nature of halophytes and glycophytes, neither can tolerate high salt concentrations in their cytoplasm; thus, the focus of most projects is on the Na⁺ ion transfer mechanism and its distribution in various parts of plants. After entering Na⁺ into cytoplasm, it is transferred to vacuole through antiporter [57]. There are two types of H⁺ pumps in vacuole membrane vacuolar H⁺-ATPase (V-ATPase) and Vacuolar H⁺-pyro-phosphatase [58]. The electrochemical proton gradient created by these two transferring enzymes in the vacuole provides the necessary power for ion transport. Under stress-free conditions, H⁺ pump plays a significant role in preserving mineral homeostasis, secondary transferring energy, and facilitation of vesicle fusion. Under salt stress, the plant survival depends on the V-ATPase pump, which is dominant in the H⁺ pump.

In another view, it is considered the vital role of salt overly sensitive gene network (SOS) to salinity for Na⁺ ion regulation and salt tolerance [59]. The SOS signaling network consisted of three main proteins SOS1, SOS2, and SOS3. SOS1 gene codes anti-porter H⁺/Na⁺ of plasma membrane, which facilitates the transport of sodium from root tissue to stem. The SOS2 gene codes serine/threonine kinase which is activated by Ca²⁺ signals. The third protein involved in SOS signaling is SOS3, which is Ca²⁺ domain binding to N⁻ terminal of SOS2. By increasing Na⁺ concentration, a severe increment of Ca²⁺ level in the intracellular area occurs, which in turn facilitates its binding to SOS3 protein. SOS3 activates SOS2 by releasing internal inhibitors. The combination of SOS2-SOS3 on plasma membrane is loaded where SOS1 phosphorylates, which causes an increase in sodium flow and a reduction in its toxicity. In legumes, the ion distribution, specifically the ratio of K⁺/Na⁺ in the cytosol, has been reported in various ways among their different species and cultivars.

For example, the response of various legumes to salt stress is determined by Cl⁻ toxicity (mungbean), Na⁺ toxicity (soybean), and Cl⁻ and Na⁺ toxicity (common bean and cowpea) [47]. In one study, it was reported that there were exceptional K⁺/Na⁺ transporters in the mash bean cultivar, which conserve lower levels of intracellular Na⁺ [60]. However, it was observed that the uptake of K⁺ resulted in the developing Na⁺/K⁺ ratio, which was regulated by a decrease of Na⁺/Ca²⁺ ratio in pigeon peas under salinity [61]. According to Zhang et al., soybean salt tolerance was obtained by plasma membrane Na⁺/H⁺ exchanger GmSOS1, which maintains Na⁺ homeostasis in soybean [62].

The mechanisms in relation to cytoplasmic Na⁺ reduction include restriction of Na⁺ uptake, increase of Na⁺ efflux, and compartmentalization of Na⁺ in the vacuole [63]. The rice plasma membrane Na⁺/H⁺ anti-porter (OsSOS1) excludes Na⁺ from the shoot, promoting a lower cellular Na⁺/K⁺ ratio and increasing salt tolerance [64, 65]. The vacuolar Na⁺/H⁺ anti-porters OsNHX1, OsNHX2, OsNHX3, OsNHX4, OsNHX5, and OsARP/OsCTP play important roles in the vacuolar compartmentalization of Na⁺ and K⁺ that accumulate in the cytoplasm and thereby determine rice salt tolerance [66]. OsHKT1;1, OsHKT2;1, OsHKT2;3/OsHKT3, OsKAT1, OsKAT2, OsHAK5, and OsHAK21/qSE3 transport Na⁺ or both Na⁺ and K⁺, helping to maintain Na⁺/K⁺ homeostasis in the cytoplasm and regulate rice response to salt stress [67].

Some genes that include transcription factors affect the salt tolerance of rice by regulating the expression of CLC, NHX, and HKT genes, activating the expression of the K⁺/Na⁺ transporter, and reducing sodium absorption into the cells [68].

4.2 Compatible solute accumulation and osmotic protection

The compatible solute (compatible osmolytes or osmoprotectants) are not toxic even at higher concentrations. Their effective role is to protect osmotic structure and balance within cells through continuous infiltration flow of water and water flow reduction. Related to their prominent feature, it can be referred to as being hydrophilic compounds with low molecular weight and no net charge at physiological pH. Under salt stress, there are various types of solute accumulation varying among different plant species including amino acids (proline), carbohydrates (sucrose and fructose), quaternary amines (glycine and betaine), ions (potassium), and organic acids (malate and nitrate) [69]. El-Sabagh et al. reported on the effect of exogenous osmoprotectants such as proline on soybeans under salinity stress in order to increase salinity resistance [70]. The accumulation of proline was observed in common bean (Phaseolus vulgaris L.) subjected to salt stress, followed by its increased accumulation in salt-stressed plants treated with effective microorganisms [71].

The other non-toxic osmolyte is beta-glycine, which raises osmorylation during stress conditions and plays an important role in osmotic adjustment [72], protein fixation [73], photosynthetic system protection [74], and reactive oxygen species (ROS) reduction [75]. Another research has demonstrated the existence of less protein and high protein and amino acids content in salt-tolerant than salt-sensitive beans [76]. In addition, it was shown that osmotic regulation in soybeans occurs by regulating the concentrations of trigonelline, proline, and potassium [70]. Also, the osmotic adjustment caused by accumulation of amino acids, reducing sugars, and ascorbic acid has been reported in pea plants subjected to salt stress [77]. Finally, osmoregulation can be controlled by various osmolytes, which are key factors to decrease osmotic stress in grain legumes.

Salt stress also causes osmotic stress and promotes the biosynthesis and accumulation of compatible osmolytes, which decrease cellular osmotic potential and stabilize cellular proteins and structures [78]. OsP5CS1 and OsP5CR proline synthesis genes increase the accumulation of proline and improve the tolerance of rice to salt stress [79]. OsGMST1, which encodes a monosaccharide transporter, increases monosaccharide accumulation and improves salt tolerance in plants [80]. It is reported that sugars will eventually be exported to transporters (SWEETs) that can regulate sucrose transport/distribution and maintain sugar homeostasis in rice under drought and salinity stresses [81]. In addition, rice glycine betaine is the other osmolyte synthesized by choline monooxygenase OsCMO, and beating aldehyde dehydrogenase OsBADH1 increases the tolerance of rice to salt stress by incrementing the accumulation of glycine betaine [82].

4.3 Regulation of antioxidants in order to tolerance to salt stress

Antioxidant metabolisms like enzymatic and non-enzymatic compounds play a critical role in preventing reactive oxygen species (ROS) resulting from salinity stress [83]. These lethal compounds contain hydrogen peroxide (H₂O₂), hydroxylradical (OH), superoxide-radical (O⁻²), and singlet-oxygen (O²), which damage cells, along with different proteins, nucleic acids, and membrane lipids, which lead to oxidative stress [84]. Salt tolerance has a positive correlation with antioxidant enzymes such as glutathione peroxidase (GPX), glutathione reductase (GR), superoxide dismutase (SOD), ascorbate peroxidase (APX), and catalase (CAT) as well as the accumulation of non-enzymatic antioxidant compounds. Under salt stress conditions, the activity of these enzymes increased in the tolerant variety [85]. In the previous research, APX and CAT activities were enhanced in bean salt-tolerant cultivars subjected to salt stress [86]. In conclusion, the enhanced activities of antioxidants in legumes perform as a protective process over oxidative stress.

Superoxide dismutase (SOD) can evacuate the surplus superoxide anions in the cells and hence act as the first line of defense. It is classified into three groups in higher plants. Based on the metal ions present on auxiliary sites, they are iron SOD (Fe-SOD), copper/zinc SOD (Cu/Zn-SOD), and manganese SOD (Mn-SOD). The SOD can dismutase the superoxide anion into the O₂ and H₂O₂ and abolish the superoxide toxicity [87].

Ascorbate peroxidase (APX) is one of the important enzymes that eradicate H₂O₂. The adverse effects of salt stress in different plant species are mitigated by exogenous application of ascorbate, and it endorses plant recovery from salt stress [88, 89].

Catalase (CAT) is another important enzyme that reduces H₂O₂ and is present in peroxisomes. It differs from APX in that it has a high affinity for hydrogen peroxide and requires a reducing substrate. Hydrogen peroxide from the light reaction is mainly removed by CAT. The effects of NaCl on H₂O₂ content and CAT activity were studied in various groups of plants, all of which show high tolerance to NaCl. In all cases, treatment of plants with high salinity levels increased H₂O₂ concentration, and as a result, CAT enzyme activity also increased [90].

A lower accumulation of O₂ and H₂O₂ was observed in overexpressing OsMn-SOD1 and OsCu/Zn-SOD lines under salt stress [91]. APX gene family in Oryza sativa increase APX activity, decrease H₂O₂ and malondialdehyde levels, reduce oxidative stress damage, and increase rice tolerance to salinity stress [92]. Glutathione responsive rice glyoxalase II in salt stress conditions with increased photosynthetic efficiency [93], the GR gene family in rice [94] and rice GDP-mannose pyrophosphorylase and dehydroascorbate reductase play an important role in increasing plant tolerance [95].

4.4 Polyamine role in salt tolerance

Polyamines are relatively polycationic low molecular weight compounds that are extremely widespread in all organisms from unicellular to multicellular including putrescine (Put), spermidine (Spd), and spermine (Spm). They are applicable at different development stages including cell division, nucleic acids stability, embryogenesis, dormancy termination, aging regulation, plant growth, and stress resistance [96]. In case of salinity, it was reported that the oxidative damage was decreased by the accumulation of putrescine in soybean [97], chickpea [98], and faba bean [99]. According to spermidine, it was exhibited that spermidine was applicable to alleviate the destructive effects of salinity condition and promote salinity tolerance in various legume species such as faba bean [100], soybean [101], and mungbean [102]. Thus, legumes make use of polyamines for their adaptation and defense mechanisms to cope with the lethal consequences of salinity.

4.5 Role of nitric oxide in salt tolerance

Nitric oxide (NO) is a volatile and small gas molecule that cause plant growth regulation, root growth development, transpiration, stomata closure, flowering, seed germination, and response to salt stress as a signaling molecule [103]. The NO effect in salt tolerance relies on the regulation of H⁺-ATPase in cell membrane and Na⁺/K⁺. Under salinity stress, nitric acid is capable of ROS accumulation followed by prevention of thiobarbituric acid and other aldehyde production to decline disturbing effect of salinity stress on cell membrane [104]. In soybean, it has been reported that the use of NO increases the activity of ascorbate peroxidase enzyme, and also, in Vigna angularis, it increases the activity of oxidant enzymes and non-enzymatic compounds [105, 106].

4.6 Hormones role in salt tolerance

It is proved that crops utilize adaptive responses against salt stress (downstream of the initial salt signaling phase), which alters plant hormone levels and the salt-induced signaling cascade. Phytohormones, endogenous chemical signals, are one of the adaptive responses that coordinate plant growth and development under optimal conditions and environmental challenges [28]. Plant hormones are chemical compounds that exist in very low concentrations and play important key roles in controlling and regulating all aspects of growth and development. Hormones are classified into two main groups containing (1) growth promoters (gibberellins, cytokinins, and auxins) and (2) growth inhibitors (ABA and ethylene) that individually affect salt stress. Among all phytohormones, ABA has a significant role in saline conditions. It is considered as the central regulator of abiotic stress tolerance in plants by up-regulation of PYR, PYL, RCAR proteins complex, protein phosphatases 2C (PP2C), ABF transcription factors, and SnRK2 protein kinases, which can decrease the preventive saline effect on growth and photosynthesis. In fact, ABA is responsible for metabolic variations, stomatal closure, and stress--responsive gene regulation under salinity condition in crops, even at high concentrations of ABA, which are more helpful in osmotic adjustment using more stress protein production and salinity adaptation. For example, Shu et al. suggested that ABA could be a potential plant growth regulator in soybeans, which could improve soybean germination under salt stress [107]. In addition, it was reported that the stomata closure occurred in response to ABA in Lupinus albus L. [108]. Thus, ABA also plays a major role in mediating physiological responses to salt stress through alteration in osmotic adjustment and photosynthetic and plant developmental growth. The ABA biosynthesis genes OsNCED3 and OsNCED5, encoding 9-cis-epoxycarotenoid dioxygenases, increase ABA levels and enhance salt stress tolerance [109]. The rice ABA receptor gene OsPYL/RCAR5 is a positive regulator of the ABA signal transduction pathway in abiotic stress tolerance [110]. OsbZIP23 gene directly affects the gene responsible for ABA synthesis and the component gene of ABA signaling and can regulate ABA signaling and biosynthesis by regulating stress response pathways [111].

In one study, it was noticed that salinity tolerance incremented by promotion of ethylene biosynthesis and signal transduction in rice, while, their inhibition increased salinity sensitivity in Arabidopsis and soybean [112]. However, in tomato, the direct ethylene precursor 1-aminocyclopropane-1 carboxylic acid (ACC) causes Na⁺ accumulation and oxidative stress in leaves and promotes leaf senescence under salinity stress [113, 114]. Meanwhile, protein salt intolerance 1 (OsSIT1) in rice increases sensitivity to salinity stress by increasing ethylene production in the plant [115]. DOF transcription factors and ethylene-responsive element binding protein (EREBP) transcription factor OsBIERF3 cause positive changes in plant root length by limiting ethylene synthesis [116].

Gibberellic acid (GA) is another important hormone that regulates plant growth and is associated with the regulation of growth under abiotic stress. Gibberellin 2-oxidase 5 (OsGA2ox5) and GA catabolic pathway genes reduce GA accumulation and increase plant salt tolerance with delayed growth [117].

In case of cytokinins (CKs), its function is to control plant adaptation to environmental stresses. In Arabidopsis, by the reduction of various levels of CKs, the salt tolerance increased [118], while it was exhibited that the exogenous CK application caused salt tolerance enhancement in Solanum melongena. Indeed, the enzyme results in CK degradation pathway called as cytokinin oxidase OsCKX2, which negatively regulates salt stress tolerance by controlling CK levels [119].

Jasmonic acid (JA) is the other hormone that reduces root length and activates antioxidant enzymes under salt stress conditions [120]. It was reported that JA accumulates endogenously in rice roots and exogenously increases salt stress tolerance in rice and wheat [121, 122].

Salicylic acid (SA) is also known as adaptive response in plants under salinity stress, which plays an important role in plant salt tolerance. Exogenous SA application in plants can control salinity conditions through (1) enhancement of antioxidant system, (2) increases in the synthesis of osmolytes, and (3) promotes photosynthesis and nitrogen fixation [123].

5. Genetic engineering for salinity stress tolerance

Salt tolerance is generally controlled by large numbers of genes and different physiological mechanisms. Recently, researchers have focused on analyzing genes controlling salt tolerance by introduction of hypothetical premise for augmentation of the stress signal system and upgrading plant tolerance to stress [124]. Genetic transformation technology allows genetic scientists to transfer genes in a precise and predictable way. Based on this, manipulation of the biosynthetic pathways involved in osmotic protection and physiological traits of plants could be efficient tools to (1) raise the level of tolerance to salinity, (2) upgrade the accumulation of molecules that remove ROS, (3) reduce the concentration of lipid peroxidation, (4) maintain the three-dimensional and functional structure of proteins, etc. [125]. To produce salt-resistant plants, plant engineering methods can be used to overexpress resistance genes. Gene expression studies using constitutive promoters provide limited biological information compared to using inducible promoters or cell type-specific promoters. In this direction, the selection of strong promoters inducing abiotic stress is very important in plant breeding programs. In addition, a wide range of stress-inducible promoters are available that vary in their ability for regulation of gene expression patterns to enhance salinity tolerance in crop plants. The selection of these promoters can significantly affect the results of a transgenic manipulation. For instance, salt tolerance is fundamentally enhanced by vacuolar Na⁺/H⁺ anti-porter gene AtNHX1 and plasma membrane Na⁺/H⁺ anti-porter gene SOS1 in transgenic A. thaliana [126]. A substantial number of genes, HKT and NHX, encoding K⁺ transporters and channels have been distinguished and cloned in different plant species. The class 1 HKT transporters, distinguished in Arabidopsis, shield the plant from the antagonistic impacts of salinity by anticipating overabundance aggregation of Na⁺ in leaves [127]. Similar results were observed in an experiment with rice, where the class 1 HKT transporter removes excess sodium from the xylem, thus protecting photosynthetic leaf tissues against the toxic agent Na⁺ [128]. Transgenic genes such as Ta-UnP, TaZNF, TaSST, TaDUF1, and TaSP can significantly increase salt tolerance in wheat [129]. Studies conducted by Sun et al. revealed that an overexpressing salt-responsive gene, ZFP179, encoding a Cys2/His2 zinc finger protein, enhanced salt tolerance in rice [130]. It has also been reported that overexpression of genes for signaling proteins such as kinases and phosphatases are involved in salt tolerance in various plants. One of these proteins is mitogen-activated protein kinases (MAPKs), which are conserved signaling proteins and play an essential role in improving plant tolerance to various stresses of crops. It was reported that different transgenic plants engineered with MAPK cascade are tolerant to salt stress [131].

6. Conclusions

Totally, various studies have been demonstrated that salt tolerance consists of different cellular, metabolical, molecular, and physiological responses in the whole plant. During evolution, plants have developed the ability to detoxify excessive levels of Na⁺ and use multiple strategies to mitigate damages resulting from salinity stress. There are various ways to decline the effects of salt stress on plant growth, which require a thorough conception of which defensive responses to environmental stresses could be more appropriate. Thus, it is indispensable to apply integrated approaches such as molecular, biochemical, and physiological techniques in order to develop salt-tolerant cultivars. A comprehensive understanding of molecular mechanisms in crop salt tolerance has been gained through the development of molecular salt tolerance markers, complete sequencing of plant genomes, and the widespread use of microarray analysis and genome editing technology. In order to create salt-tolerant crops using genetic engineering methods, various tools and techniques could be distinguished, including an extensive number of salt-responsive genes, methods of gene transfer, and their promoter sequences. These powerful techniques can offer advantages and solutions to the complex and fascinating traits involved in salt tolerance plants.