Keywords

14.1 Introduction

In the last few decades, we witnessed substantial increase in productivity of food grains, oilseeds, pulses and cash crops mostly through adoption of intensive agriculture, viz. high-yielding varieties, precise fertilizer and nutrient management practices, more efficient crop protection measures, etc. But, with the continuous increase in global population by every passing year, there is an estimated need to produce 87% more food crops such as rice, wheat and maize by 2050 over that we are producing today (FAO 2017). As the horizontal area expansion in fertile agricultural land almost came to a saturation in most countries, there is a current shift in encompassing more and more nontraditional areas under cultivation to cater the global food demand. Despite the much advancement in agricultural science in all over the world, abiotic stresses still cause havoc on cultivation due to its widespread and unmanageable nature, including salinity, drought, heat and cold, critically threaten crop production and result in substantial yield loss in large arable land worldwide. Among these, soil salinity is one of the prime environmental constraints to crop production and is further expected to increase due to global climate changes (increase in coastal salinity mainly due to the rise in mean sea level) and as a consequence of injudicious and/or faulty irrigation practices. As per the recent estimate, about 800 million hectares of land globally is affected by salinity (FAO 2017). On an average 2,000 ha of irrigated land across 75 countries has been degraded by excess salt annually owing an estimated economic loss in the tune of US$ 12 billion (Ghassemi et al. 1995).

Soil salinization is a worldwide problem for agriculture affecting 6% of total Earth’s land, as a result of natural accumulation over long periods of time (Rengasamy 2002). However, agricultural activity contributes to secondary salinization: 2% of all dry land is becoming salinized, and more than 20% of irrigated soils are affected, mostly because of irrigation water containing small amounts of sodium chloride (Tester and Davenport 2003). Saline soils in general affect plant growth negatively and may even have a lethal effect causing programmed cell death upon extended exposure to high salinity. Based on the ability to tolerate NaCl concentrations, plants can be classified into two groups: glycophytes or salt-sensitive species (which are unable to tolerate even mild levels of salinity for longer periods of time) and halophytes or salt-tolerant species (which are capable of growing and thriving under high salinity). Primarily, excess salt in the soil decreases the water potential in the rhizosphere region, rendering plants unable to absorb water even in the absence of actual limitation of water quantity, a soil condition termed as physiological drought. As a result, many plant processes, viz. at the cellular level including cell enlargement, cell division, cell wall properties, etc., as well as various leaf parameters such as colour, succulence, necrosis, etc., and at whole-plant level, shoot/root ratio, growth and yield get affected (Hasegawa et al. 2000).

For most of the glycophytes, highly saline growing environment adversely affects the germination process, plant growth and metabolism as well as the overall physiology by causing ionic and osmotic stresses (Iterbe-Ormaetxe et al. 1998). Salt stress is often noted as a causal factor for increased respiration rate and ion toxicity while subsequently altering the C and N metabolism in plant cell (Kim et al. 2004). Additionally, mineral distribution and membrane instability (Marschner 1986) along with permeability (Gupta et al. 2002) and decreased biosynthesis of chlorophyll pigments and photosynthetic inefficiency (Munns 2002), all of which are caused by salt stress, collectively lead to impaired economic crop productivity. Stress-induced build-up of sugars and other compatible organic solutes is a common phenomenon for most of the abiotic stresses including soil salinity. They can serve as osmoprotectants, thus helping in stabilizing biomolecules under stress conditions. Although accumulation of ions for osmotic adjustment is energetically more preferable, many plants accumulate organic osmolytes (proline, betaine, polyols, sugar alcohols and soluble sugars) to counteract osmotic stresses. Both glycine betaine and trehalose serve as major osmoprotectants which stabilize the quaternary structures of proteins and highly ordered cellular and intracellular membranes. Proline acts as a sink for carbon and nitrogen and scavenger of free radical, which stabilizes subcellular structures (membranes and proteins) and maintains cellular redox potential (Reviewed in Chakraborty et al. 2013).

Salt stress also induces accumulation of reactive oxygen species (ROS), causing oxidative damage to cellular macromolecules, viz. proteins, membrane lipids and nucleic acids. Detoxification of these ROS is absolutely essential for plants to survive under salinity stress. To counterbalance the ROS production and oxidative stress, plants produce either molecular antioxidants for direct scavenging of these ROS or detoxify them via coordinated network of antioxidant enzymes, viz. superoxide dismutase, catalases, peroxidases and enzymes of ascorbate-glutathione cycle. Under various abiotic stresses, the activity and expression levels of genes encoding ROS-detoxifying enzymes were reported to be enhanced by oxidative stress (Abogadallah 2010; Chakraborty et al. 2016a).

Ionic homeostasis or regulation of Na+/K+ balance inside metabolically active tissue is still considered to be the most important criteria for salt tolerance (Munns and Tester 2008). Exposure to higher levels of salt stress, particularly NaCl, affects uptake of water and dissolved nutrients resulting in impaired plant water status and creates ionic imbalance by means of the cellular accumulation of toxic Na+ and Cl− ions. Sodium ions if accumulated in the cytoplasm can become extremely toxic to living cells showing their adverse effects on K+ nutrition and other pivotal plant physiological mechanisms like activity of cytosolic enzymes, photosynthesis and metabolism (Shabala and Cuin 2008; Degl’Innocenti et al. 2009). Besides, salt stress heavily tolls on the ionic homeostasis of other complementary ions such as Ca2+, Mg2+ and NO3 − , and therefore, further investigation requires altered transport and compartmentation mechanism of these nutrients under salinity stress. In plants, predominantly three distinct but complementary mechanisms operate cooperatively that selectively inhibit the accumulation of Na+ in the cytoplasm following one or other processes, i.e. checking of Na+ influx, promotion of active Na+ efflux and sequestration of Na+ in the vacuole, which will be discussed categorically in this compilation. But before that we need to understand various soil-related factors affecting availability of nutrients under salt stress.

14.2 Soil-Driven Factors Affecting Nutrient Availability Under Salt Stress

14.2.1 Salinity: Origin and Extent

Salinity is predominant in two major forms over the land surface, (1) dry land salinity and (2) irrigation salinity, and arid and semiarid climatic regions throughout the world are suffering due to salinity in one form or another. The dry land salinity is often detected as primary or secondary salting, either occurring naturally (naturally occurring saline wet and dry lands including salt lakes, salt pans, salt marshes and salt flats) or via secondary salting that is induced by human activities such as agriculture (Fig. 14.1). Secondary salinity is majorly caused by anthropogenic activities, while practising land development and agriculture may play some role (Queensland Government 1995–2017), and the common forms are:

  • Irrigation: prevalent in irrigated agricultural lands, due to excessive irrigation (results into rising groundwater tables) or the application of poor-quality water.

  • Dry land: prevalent in rainfed or nonirrigated landscapes, generally as a result of deforestation and land-use changes. Irrigation salinity often resembles dry land salinity, except that inclined level of groundwater that also resulted in deposition of salt layers in the plant root zone or on the soil surface.

  • Sea water intrusion: In coastal aquifer systems, it is commonly found that fresh groundwater is gradually replaced by sea water.

  • Point source: originated from the high concentration of diluted salt in effluent either released from intensive agriculture loaded with pesticide/chemical residues or from polluted wastewater stream from industries.

Fig. 14.1
figure 1

Causes of different types of salinity resulting in ionic imbalance in soil

Full size image

Over the years, several estimations have been published regarding the extent of salinity. Oldeman et al. (1991) reported that the total area affected by waterlogging was over 10 m ha and that affected by salinity was over 76 m ha. They counted both irrigated and rainfed areas. Dregne et al. (1991) published that about 43 m ha of irrigated land in dry lands was affected by several forms of degradation, including waterlogging, salinization and sodicity. Umali (1993) estimated that 1–1.5 m ha of lands were lost to salinization every year. Further it had been reported that nearly 12 m ha of irrigated land may have phased out from production due to salinization (Nelson and Maredia 2001). An approximate area of 7 m ha of land is estimated to be under saline soil in India (Patel et al. 2011). These lands are classified in Table 14.1.

Table 14.1 Classification of salt-affected soil
Full size table

14.2.2 Salinity Impacts on Crop Production

Agriculture is one of prime importance as far as salinity hazard is concerned. Crops may differ in their tolerance to salinity, and some of them are extremely sensitive, while few perform better even after crossing the threshold of marginal salinity and emerge as tolerant crops in terms of salinity stress. Even varietal differences are also prominent in major field crops. A report published from World Bank showed the degree of loss and major impacts due to salinity or other forms of soil degradation as a whole (Table 14.2; Fig. 14.2).

Table 14.2 Impact of soil degradation on Indian agriculture
Full size table
Fig. 14.2
figure 2

The most promising impacts of soil salinity (FAO 2017)

Full size image

14.2.3 Salinity Impacts on Nutrient Mobility in Soil and Plants

Besides the crop yield perspective, soil salinity has its own demerits creating problems like nutrient loss, nutrient imbalance, poor soil structure and health, and soil degradation. Dry land salinity is often considered as a major soil degradation issue, including soil erosion. Salinity is often associated with prolonged wetness, sparse vegetation and lack of surface cover and therefore increases the vulnerability of soils to erosion. Salt concentration in the soil solution (salinity) which governs the osmotic potential and the concentration of sodium on the exchange complex sites (sodicity) further determines soil structural stability. Thus, salinity slowly turns into sodicity. The major soluble salts in soils are the cations like Na+ (sodium), Ca2+ (calcium), Mg2+ (magnesium) and K+ (potassium) and the anions like Cl− (chloride), SO4 2− (sulphate), HCO3 − (bicarbonate), CO3 2− (carbonate) and NO3 − (nitrate) (Shi et al. 2005). These are the basic ions that dominate in the exchange sites under salinity and thus compromise the places of other essential nutrients like PO4 3− (phosphate) and micronutrients (Zn, Fe, Mn, Cu). This imbalance of nutrients created in soil is often measured by nutrient concentration or uptake by plants comparing the plants grown under normal and saline conditions. Similar occurrence was reported by Bhaduri et al. (2016) where P uptake of eight groundnut cultivars were studied and observed that the P uptake of groundnut cultivars is affected at irrigation salinity level of 6.0 ECiw. Salinity stress lowered down the N content in Brassica leaves as well as seed protein content; moreover the reduced accumulation of micronutrients (Fe, Mn, Zn) was also noticed in the leaf, stem and root at flowering and post-flowering stages (Chakraborty et al. 2016b).

Soil microorganisms, an integral component of soil ecosystem, are largely involved in an array of important soil nutrient cycling processes. Their roles in nitrification, ammonification, nitrogen fixation, P mineralization, S oxidation, decomposition of soil organic matter and transformation of all primary and secondary nutrients (Amato and Ladd 1994) are already established. Microbes also act in formation of humic substances which makes stable forms of organic C and contribute in C sequestration in soils. The high concentration of soluble salts affects the microbes by increasing the osmotic potential (more negative) of the soil water, promotes exosmosis and dehydrates the microbial cell. Thus, it makes difficult for microbes to survive and perform their basic functions in a saline soil. Even if they can survive under such stressful situation that needs more investment of energy for producing osmolytes. Till date, only few halophytic microbes and some endophytes are reported to tolerate such extreme saline conditions. Moreover, soil microbial community structure also differs significantly since fungi are more salt sensitive over bacteria, and thus bacteria/fungi ratio can be increased under saline soil environment (Wichern et al. 2006; Yan et al. 2015). All these phenomena either singly or collectively influence the soil nutrient availability.

14.3 Uptake of Regulatory Ions in Plant Cells: An Interplay of Nutrient Balance/Imbalance

Salinity is a much complex phenomenon rather than a simple escalation in the concentrations of sodium and chloride ions inside the plant tissue (Nouri et al. 2017). Apart from Na+ and Cl−, number of other cations and anions, viz. calcium, carbonates and sulphates, may be present in disproportionate amounts and play crucial role in negatively affecting plant growth (Gorham 1992). Simultaneously, certain nutrients (particularly potassium, nitrogen and phosphorus) may be available or present in such low amounts under saline condition that they might hamper proper growth (Chakraborty et al. 2016c).

Saline conditions affect plant growth and metabolism in many different ways. These harmful effects are generally associated with (1) reduced osmotic potential of the soil solution in plants (water stress), (2) nutritional imbalance, (3) effect exerted by a specific salt (salt stress) or (4) a combination of all of these factors (Ashraf and Foolad 2007; HanumanthaRao et al. 2016). These factors act in an adverse way affecting growth and development in plants at both physiological and biochemical levels (Munns 2002; Munns and Tester 2008) and also at the molecular level (Tester and Davenport 2003). Tolerance to saline conditions involves a myriad number of physiological processes manifested in numerous levels of organization, viz. alterations in gross morphology, tissue partitioning and coordinated control of transport, biological change for maintenance of protein structure and regulated transcriptome level changes (Tester and Davenport 2003).

14.3.1 Scenario of K+ vs Na+ and K+/Na+ Homeostasis Under Salt Stress

Sodium, an integral constituent of our Earth’s crust, is naturally present in all soil types. At lower concentration Na+ helps in supporting growth and development for some plants, but at higher concentration in soil or other growing medium, it eventually turns out to be toxic to even glycophytes (Flowers and Colmer 2008). Both Na+ and K+ share high similarity in ionic as well as its chemical and structural properties, but unlike Na+, K+ are integral part of plant’s life and play essential role in growth and development (Schachtman and Liu 1999). Many core physiological processes, primarily dependent on K+, show impairment due to hindrances in specific transport and interactions of K+ with enzymes and membrane proteins (Britto and Kronzucker 2008). This may be manifested as transient maintenance of membrane potential for stomatal movement and development of pollen tube in plants (Dietrich et al. 2001). Under saline condition, due to prolonged exposure to salt stress, plants often exhibit K+ deficiency symptoms majorly because of reduced uptake by the root tissue and/or lesser K+ retention in different plant parts coupled with a concomitant accumulation of tissue Na+ concentration (Munns et al. 2002). Under salt stress, plants with hindered growth and metabolism are observed due to the skewed K+/Na+ ratio in metabolically active plant tissues (Shabala and Cuin 2007; Degl’Innocenti et al. 2009). Because of such ionic imbalances, hindrances in various physiological and biochemical processes are observed in plants.

Under high external Na+ concentrations, Na+ enters through K+ pathway altering the ion ratios in plants. The similarity of the ionic radii of the hydrated molecule of Na+ and K+ renders the capability of discrimination between them much difficult and hence forms the basis of Na+ toxicity. Cellular K+ concentrations in the range of 100–150 mM are essential for in vitro protein biosynthesis. Moreover, at higher concentrations, Na+ competes for K+ sites and inhibits the whole process when Na+ concentrations is >100 mM (Cheeseman 2013). The similar level of sensitivity of cytosolic enzymes of halophytes and glycophytes towards saline conditions hinders the adaption of halophytes to high salt concentration (Flowers et al. 2014). Maintenance of low cytosolic Na+ concentrations and a high cytosolic K+/Na+ ratio is a key strategy adapted by plants to respond to elevated external Na+ concentrations (Blumwald et al. 2000). The approach towards such maintenance involves extrusion of Na+ or its compartmentalization mainly in the vacuoles for metabolism (Zhu 2003) and is critical for the detoxification of excess Na+ present in cytosol and the osmotic adjustment necessary to endure salt stress (Blumwald et al. 2000; Chakraborty et al. 2016d).

14.3.2 Regulation of Tissue Na+ Concentrations

14.3.2.1 Sodium Uptake

On exposure to salt stress, maintenance of low concentrations of Na+ and high concentrations of K+ in the cytosol becomes crucial and is achieved by controlled expression and activity of K+ and Na+ transporters (Shabala et al. 2015). Na+ enters the plant cells passively through the high-affinity K+ transporter HKT1 (Rus et al. 2001; Maser et al. 2002) and non-selective cation channels (NSCCs). Due to non-selectivity of a few transporters and/or ion channels, under highly saline conditions, Na+ ions compete with K+ ions for uptake and enter inside the plant through normal rhizospheric nutrient uptake process. At transcriptional level, these K+/Na+ transporter genes are either up- or downregulated as a response to salt stress (Chakraborty et al. 2016e). It has been reported that the transcript level of Arabidopsis root K+ transporter AtKC1 increases under salt stress (Pilot et al. 2003). As reported by Zhu (2003), upregulation in the expression level of KMT1 (a AKT/KAT family member) and various HAK/KUP (high-affinity K+ transporter/K+ uptake transporter)-type genes was observed, whereas for MKT1 (another AKT/KAT family member), the expression level was found to be downregulated for common ice plant.

14.3.2.2 Sodium Efflux

The primary mechanism of Na+ extrusion in case of plants is mediated by energy-driven active pumping out of Na+ by plasma membrane-bound Na+/H+ transporter and H+-ATPases (Zhu 2001). The H+-ATPase acts to pump H+ out of the cell using the energy of ATP hydrolysis, thus generating an electrochemical proton gradient. The proton-motive force thus generated is further required for the Na+/H+ antiporter operation as the inward movement of H+ along with the electrochemical gradient is coupled to the outward exclusion of Na+ against the electrochemical gradient. Confirmation of the existence of such biochemical mechanism has been documented for various plant species (Blumwald et al. 2000). Identification of a putative Na+/H+ antiporter with substantial similarity in sequence with plasma membrane Na+/H+ antiporters from bacteria and fungi has further strengthened the views. The SOS1 (salt overly sensitive 1) locus encoding a putative Na+/H+ antiporter having considerable sequence similarity to plasma membrane Na+/H+ antiporters from bacterial and fungal species has been identified in Arabidopsis (Shi et al. 2000), rice (Martinez-Atienza et al. 2007), wheat (Yang et al. 2009) and in Brassica (Chakraborty et al. 2012a).

14.3.2.3 Vacuolar Sodium Compartmentation

It has been observed that both halophytes and glycophytes regardless of the high influx of Na+ maintain the cytosolic concentration of the ion at non-toxic levels (Blumwald et al. 2000). The compartmentalization of Na+ into vacuoles has been found to be the primary mechanism of evading the harmful effects Na+ exerts in the cytosol. Additionally, the vacuolar compartmentalization of Na+ (and Cl−) allows the usage of NaCl as an osmoticum thereby contributing in maintenance of an osmotic potential for the process of water uptake into cells (Blumwald et al. 2000). Tonoplast-bound vacuolar Na+/H+ antiporters (NHX family transporters) play crucial role in Na+ compartmentalization inside the cell (Yokoi et al. 2002). Identification and characterization of several plant transporters have been made possible by detection of the higher degree of homology between several plant and yeast genes, and the detailed genetic information is available in the public domain (Halfter et al. 2000; Ji et al. 2013). Evidences suggest that Na+ detoxification mechanisms employed in yeast cells may be found to be quite similar to that existing in plant cells. This similarity mostly holds true for the role played by the Ca2+-dependent signal transduction mechanism which becomes operational under salinity stress (Halfter et al. 2000). Putative Na+/H+ antiporters (both SOS1 and NHX family) from both organisms are also similar (Apse et al. 1999; Fukuda et al. 1999).

14.3.3 Interaction Between Na+ and Ca2+

An important inorganic nutrient, calcium, plays a vital role in salt detoxification, in addition to its well-known metabolic and structural functions (Jin et al. 2007). This response stems from the fact that increasing Na+ concentrations may not only reduce Ca2+ availability but may also displace Ca2+ from its extracellular binding sites within the plant organs and further disrupt Ca2+ acquisition (Hadi and Karimi 2012). The interaction between Na+ and Ca2+ in salt-stressed plants has been the focus of several research agendas over the years (Cramer 2002; Nedjimi and Daoud 2009). It has been advocated that Na+ tolerance of plants is determined to a larger extent by interactions of Ca2+ and Na+ ions (Buschmann et al. 2000). It is reported that high NaCl induces calcium deficiencies in different plants such as Vigna unguiculata (Murillo-Amador et al. 2006) and tomato (Tuna et al. 2007). Allen et al. (1995) reported that Na+ influx on durum wheat cells can also be inhibited by calcium. According to Jin et al. (2007), saline conditions restricted Ca2+ uptake by the roots of Aloe vera plants and its subsequent transport to shoots resulting in a marked decrease in Ca2+ contents of all plant parts. It was further reported that in plants under salt stress, the Ca2+ contents of the leaves and stems show a noticeable decrease; salt-tolerant genotypes were found to exhibit three times higher Ca2+ concentrations as compared to salt-sensitive ones.

High Na+ concentration in the root zone was found to inhibit Ca2+ uptake and its transport resulting in lower Ca2+/Na+ ratios in salt-stressed plants (Hadi et al. 2008). Additionally, Jin et al. (2007) showed that salt-tolerant genotypes of Aloe vera maintained a significantly low Na+/Ca2+ ratio and experienced least membrane damage. The rapid Na+ uptake process across the plasma membrane in excess salt condition diminishes the binding capability of Ca2+ to the plasma membrane thus inhibiting its influx. High Na+ concentrations can displace Ca2+ in membrane thus disrupting the integrity of it (Janicka-Russak and Kłobus 2007). Hasegawa et al. (2000) in their report indicated that the increase in intercellular Ca2+ content could cause a decline in Na+ influx and in turn increase the K+ selectivity for absorption thus alleviating the damaging effects of salinity stress. They also pointed out that under salinity stress, Na+ can compete with Ca2+ by entering the cell through the same channels. The excess intercellular sodium can then displace the Ca2+ in the membranes causing membrane damage. Membrane-bound catalase activity could also be inhibited by excess Na+ which can be reversed by excess Ca2+ (Arbona et al. 2003). It has been proposed that Ca2+ plays a central role in plants exposed to NaCl salinity because of its active participation in reducing Na+ absorption and increasing potassium (K+) and Ca2+ uptake, resulting in an increase in plant growth (Caines and Shennan 1999). Additionally, Ca2+ may compete with Na+ for membrane-binding sites thereby shielding the cell membrane from the unfavourable saline conditions (Shabala et al. 2006).

The [Ca2+]ext augments salt tolerance by eliciting a transient increase in [Ca2+]ext either from a peripheral or an internal source (Knight et al. 1997). Experiments conducted on yeast have generated preliminary views of Ca2+-mediated activation of signalling pathways for regulation of ionic homeostasis and tolerance mechanisms in response to salt stress conditions. A suggestive model for salt-induced Ca2+ signalling and activated SOS pathway includes components of the SOS pathway; the SOS3 or other upstream elements might become connected with the osmotically responsive channel triggering Ca2+ influx which might possibly initiate signalling through the pathway (Chakraborty et al. 2016e). Reports suggests that salt-induced [Ca2+]ext transient as well as the new [Ca2+]ext steady state may be influenced by the ECA and ACA Ca2+-ATPases as well as the CAX1 and CAX2 transporters, the orthologs of VCX1P (Sze et al. 2000). Ca2+ plays two vital roles in conferring tolerance towards salinity, the fundamental signalling function leading to adaptation during salt stress conditions and a direct inhibitory effect on the entry of Na+ ions.

14.3.4 Transport and Xylem Loading

Na+ transport across the root and into the xylem occurs both symplastically and apoplastically from the epidermis to the xylem (Maathuis et al. 2014). Na+ export to the xylem is supposed to be an active process, given that the electric membrane potential of xylem parenchyma has been found to be negative. In Arabidopsis, under the conditions of salinity, xylem loading of Na+ was found to be mediated by SOS1 (salt overly sensitive1), while its unloading, on the other hand, was found to be a passive process, involving transportation through the Na+-permeable channels (Apse and Blumwald 2007). High-affinity K+ transporters or HKTs, classified in class I and class II types, were one of the most studied Na+-permeable transporters in plants (Horie et al. 2009). These HKT transporters, often located in the xylem parenchyma and root epidermal cells of many plants, exhibit a crucial role in adapting the plant to saline conditions for both mono- and dicotyledonous species (Møller et al. 2009; Munns et al. 2012). The class I HKT transporters showing specificity for mostly Na+ ions are characterized as low-affinity transporters (Munns and Tester 2008). Among the different subtypes of HKT1 transporter, a few are reported to be located in the plasma membrane of root stele cells, particularly in the xylem parenchyma cells (XPC), where their main function is to regain the Na+ ion from the xylem sap thereby avoiding transport and accumulation of toxic Na+ in the above ground plant parts and preventing damage to the more sensitive and photosynthetically active tissues (Ren et al. 2005).

14.4 Mechanisms of Nutrient Homeostasis: A Balancing Approach of Plants Facing Salt Stress

Physiological studies carried out in many crops during salt stress at vegetative stage indicated that stress tolerance trait inversely correlates with shoot Na+ concentration and Na+/K+ ratio (Ashraf 2004; Negrão et al. 2011). Different mechanisms associated with salt tolerance in crop plants include (1) maintenance of a more negative membrane potential, (2) intrinsically higher H+-ATPase activity, (3) extrusion of Na+ from the cytosol to the external medium, (4) maintenance of mineral nutrient homeostasis, particularly, higher selectivity to K+ and Ca2+ over Na+, (5) scavenging of ROS, (6) accumulation of compatible solutes for osmotic adjustment, etc. At the physiological level, salt tolerance and ion homeostasis are mostly governed by three major strategies in crop plants: (I) Na+ exclusion, (II) K+ retention and (III) tissue tolerance/Na+ sequestration (Munns and Tester 2008).

14.4.1 Electrophysiological Basis of Salt Tolerance: Role of Transporter/Pumps/Ion Channels

Plant salinity stress signalling is a complex phenomenon involving the interplay of many biomolecules ranging from receptor molecules, ion fluxes that serve as signals, transcription factors, hormones, reactive oxygen species (ROS) and numerous downstream proteins. In the cyanobacterium, Synechocystis sp., Marin et al. (2003) identified sensory histidine kinases, namely, HIK16, HIK33, HIK34 and HIK41, involved in the perception and transduction of salt stress. In plants, there is less clarity about the proteins that perceive salt stress. Salt overly sensitive (SOS) genes (SOS1-SOS4), first identified in Arabidopsis thaliana through positional cloning, are potential candidates for detecting elevated Na+ concentrations in intracellular and extracellular sites. The AtSOS1 protein is a putative plasma membrane Na+/H+ antiporter that regulates plant Na+ homeostasis by extrusion and is aided in its function by two other proteins SOS2 and SOS3 (Qiu et al. 2002; Zhu 2003). SOS-mediated salt stress signalling is represented in Fig. 14.3. The sos1, sos2 and sos3 mutants show salt sensitive phenotype, and their genetic analysis has helped to improve our understanding of the mechanism of salt stress tolerance in plants (Zhu et al. 1998). Yeast mutants lacking endogenous Na+ transporters were used to investigate the role of the three SOS proteins in salt-stress response pathway (Quintero et al. 2002). Perception of salt stress is followed by subtle changes in Ca2+ concentration in cytosol of root cells that triggers the SOS pathway (Guo et al. 2004; Chinnusamy et al. 2005). SOS3 is a myristoylated Ca2+-binding protein that recruits SOS2 serine-threonine protein kinase to the plasma membrane after binding of Ca2+ (Ishitani et al. 2000; Halfter et al. 2000). An alternative regulator of SOS2 activity, SOS3-like calcium-binding protein 8 (SCaBP8, a.k.a. calcineurin B-like CBL10), has been shown to function primarily in the shoots of Arabidopsis, while SOS3 expresses predominantly in roots (Quan et al. 2007). SOS2-mediated phosphorylation of SCaBP8 or SOS3-like proteins increases their stability (Lin et al. 2009). The SOS3-SOS2 or SCaBP8-SOS2 complex then recruits SOS2 to plasma membrane to activate downstream SOS1, which functions to extrude excess Na+ from the cytosol (Shi et al. 2000; Qiu et al. 2002; Quintero et al. 2002, 2011; Quan et al. 2007). SOS4 and SOS5 also play important roles in salt stress tolerance. While SOS4 encodes a pyridoxal kinase that is involved in regulation of Na+ and K+ homeostasis (Shi et al. 2002), SOS5 aids in the maintenance of normal cell expansion during stress (Shi et al. 2003).

Fig. 14.3
figure 3

A coordinated network of Na+ and K+ transport in different plant parts under salinity stress

Full size image

Other Na+ transporters functioning in salinity tolerance include those involved in intracellular compartmentalization of Na+ into vacuoles, older leaves or leaf sheath, extrusion outside the cell and recirculation of Na+ out of the shoots to be stored elsewhere, for example, in roots or stem cell vacuoles. Vacuolar Na+ sequestration is one of the most energetically efficient mechanisms by which plants achieve turgor maintenance and cell expansion in saline conditions. The NHX-type intracellular Na+/H+ exchangers that mediate this process are driven by the differential proton (H+) gradient generated by vacuolar H+-translocating enzymes such as H+-ATPase and H+-PPase. Plant NHX family can be divided into two groups, class I and class II, based on protein sequence and subcellular localization (Rodriguez-Rosales et al. 2009; Pardo et al. 2006). The class I NHX proteins are located on the tonoplast, where they function as (Na+, K+)/H+ antiporters (Venema et al. 2002), while the class II NHX proteins are located in endosomal vesicles of plants (Bassil et al. 2011). These proteins maintain K+ homeostasis and function in aiding normal plant growth and development as well as tolerance to salt stress (Pardo et al. 2006). The AtNHX1 gene, the first plant member of the NHX subfamily of intracellular Na+/H+ antiporters from Arabidopsis thaliana, was identified based on its homology to animal plasma membrane Na+/H+ antiporters of the NHE family and the yeast ScNHX1 gene (Gaxiola et al. 1999). Overexpression of AtNHX1 in other plant systems led to improved salt stress tolerance (Zhang and Blumwald 2001; Zhang et al. 2001). A different model for the role of NHX transporters has been proposed by Jiang et al. (2010), which states that the NHX proteins function mainly to prevent toxic Na+/K+ ratios in the cytosol and for maintaining osmotic balance which is achieved by the vacuolar compartmentalization of Na+ and, in some cases, of other cations as well. A wheat NHX antiporter, TaNHX2, having significant sequence homology to NHX sodium exchangers as reported from Arabidopsis, was found to suppress the salt sensitivity of a yeast mutant strain by improving its K+ content when faced the salt stress (Xu et al. 2013). Here an attempt had been made to compile reported transporters/ion channels/ pumps associated with movement of Na+ and K+ in plants (Table 14.3).

Table 14.3 A glimpse at the probable transporters playing a role in salinity tolerance with inputs from Almeida et al. (2013, 2017), Maathuis (2006), Kumar and Mosa (2015) and Shabala and Pottosin (2010)
Full size table

14.4.2 Transcription Factor (TFs) Involved in Salinity Stress Tolerance and Ion Homeostasis

In order to impart enhanced salt tolerance, it is essential to develop a basic understanding of biochemical, physiological and gene regulatory networks of stress response pathways. Transcription factors (TFs) play a critical role in signal transduction network starting from the perception of stress signal to the expression of stress-responsive genes. Unlike the structural genes, TFs tend to control several complex pathways (master regulator) making them one of the ideal candidates for pathway manipulation. Several TFs (OsRAB1, MYC/MYB, OsNAC/SNAC, etc.) have been identified which are differentially expressed during adaptation to salt stress; interestingly, many of these TFs are also differentially expressed during other stresses. In particular, there are many common TFs that control gene expression both during salt and drought stress. A comprehensive database of rice TFs involved in adaptation of salt and drought is available at Rice Stress-Responsive Transcription Factor Database (RiceSRTFDB; http://www.nipgr.res.in/RiceSRTFDB.html) (Priya and Jain 2013). A recent study on transcriptome analysis of common bean (Phaseolus vulgaris L.) under salt stress has reported differential expression of 59 different families of TFs among which 10 TF families, viz. AP2-EREBP, bHLH, PHD, HB, (R1)R2R3_Myb, WRKY_Zn, NAC, bZIP, C3H-TypeI and Myb_related, were most abundant (Hiz et al. 2014). A comparison of transcriptome of salt-sensitive (Hua 30) and salt-tolerant (Hua 11) barley varieties under salt stress has also shown differential expression of several transcription factors belonging to different families, such as TIFY (earlier known as ZIM), WRKY, zinc finger, MYB, bHLH, CBF, NAC, bZIP, AP2, whirly, HD-ZIP, etc. Two interesting observations of this study were that (i) the number of differentially expressed genes was more in shoots as compared to roots and (ii), compared to control, more number of genes were found to be upregulated in response to salt stress than downregulated (Gao et al. 2013). Cloning and validation of such salt stress-responsive TFs is a step in the right direction for improvement of salinity tolerance in crops. For example, stress-specific NAC1 (SNAC1) cloned from rice landrace Pokkali (Hu et al. 2006) was found to confer salt stress tolerance in rice by working downstream to ABA-induced salt and drought tolerance pathway (Khong et al. 2008). Similarly, OsMYB48-1 conferred tolerance to salt stress along with drought in rice (Xiong et al. 2014). On the other hand, cold-induced MYB 1 (CMYB1) which is involved in cold tolerance and circadian rhythm maintenance in rice is negatively correlated with salt stress tolerance. Many of these cloned TFs are trans-acting, i.e. they can impart salt tolerance in different (non-native) backgrounds. For example, OsDREB2A, a transcription factor of AP2/ERF family in rice is capable of imparting salt tolerance in transgenic soybean by accumulation of higher level of osmolytes (Zhang et al. 2013). Some of the other such transacting TFs are OsMYB3R-2 (Dai et al. 2007), HvCBF4 (Oh et al. 2007), DREB1A (Oh et al. 2005), NAC (Tran et al. 2004), etc. If regulated properly in the transgenic background, these trans-acting TFs can work to regulate pathways in any of the desired crops and thus be ideal candidates for engineering salt stress tolerance in crop plants.

14.4.3 Post-transcription Gene Regulation and Adaption to Salt Stress

Apart from the transcription factors, which play a role as master switches to control and coordinate transcription of several genes, a plethora of genes are also controlled post-transcriptionally under salinity stress. This post-transcriptional regulation is achieved through a group of salt-responsive microRNAs (miRNAs), a class of small non-coding RNAs of ~21 nucleotide length, which exerts an additional level of control over plant gene expression under stress. In fact, miRNAs are now considered as one of the major players in gene regulation which downregulate expression of their target genes by mRNA cleavage or translation-arrest mechanisms based on the perfect or near-perfect complementary pairing, respectively (Ambros 2004). A plethora of miRNAs have been demonstrated to play a role in several stress tolerance pathways; some of them are found to be involved in multiple stresses and across species (Dugas and Bartel 2004; Zhang and Wang 2015). Till date, about 40 different families of miRNAs have been shown to play a role in abiotic stress response among which many are associated with salt stress (Covarrubias and Reyes 2010; Sunkar 2010; Wang et al. 2013). Arabidopsis and rice have come up as a model system in recent times to study molecular biology of dicotyledonous and monocotyledonous plant systems, respectively. Numerous studies on these two plants have revealed the importance miRNAs in salt responses. Apart from these, the role of miRNA under salt stress has also been elucidated in several other crop plants like cotton, soybean, Populus, tobacco, Medicago, etc. About 217 miRNAs have been reported till date in different plant species which are involved in salinity stress. A detailed list of the salt-responsive miRNA and their target genes is given in Mittal et al. (2016). The unifying themes which emerge from the studies investigating the role of miRNA in response to salinity are summarized here. Firstly, it has been observed that miRNAs, grossly, target master switches of gene regulation such as transcription factors (e.g. MYB, NAC1, homeodomain-leucine zipper, etc.) or phytohormones (auxin, GA, ethylene and ABA signalling) which in turn regulate expression of several downstream genes in the expression cascade ultimately governing the plant development and physiology (Jones-Rhoades and Bartel 2004). Besides, some of these miRNAs regulate enzymes such NADP-dependent malic enzyme, cytochrome oxidase, laccase, etc. which are of broad spectrum and are involved not only in salt stress but also in several other abiotic and even in biotic stresses (Yan et al. 2005). Hence, most of the miRNAs are not specific to salt but are involved in multiple stresses; especially, several miRNA are commonly regulated in salt and drought stress (Kong et al. 2010; Xie et al. 2014). Secondly, it has been found that the stress-responsive miRNAs are more or less conserved in plant kingdom. For example, miR393 was found to be upregulated in rice, cotton and Arabidopsis under salt stress (Sunkar and Zhu 2004) and subsequently regulates auxin signalling in those plants (Xia et al. 2012). Similarly, salt-induced upregulation of miR156 is observed in seven different species, viz. Arabidopsis thaliana (Liu et al. 2008), Zea mays (Ding et al. 2009), Populus euphratica (Qin et al. 2011), Vigna unguiculata (Paul et al. 2011), Panicum virgatum (Sun et al. 2012), Populus trichocarpa (Li et al. 2013) and Gossypium raimondii (Xie et al. 2014). Several other miRNAs like miR159, miR160, miR162, miR164, miR166, miR167, miR168, miR169, miR395, miR397, etc. are also differentially expressed in multiple species under salt stress (Mittal et al. 2016). Combining these two facts, i.e. the evolutionary conserved nature and the overlapping expression pattern of miRNA in different stresses, it is intimidating to speculate that the miRNA-mediated gene regulation is an ancient phenomenon (relics of RNA world hypothesis?) which has probably originated as early as the plant kingdom made their existence in the world. And this regulation mechanism is not stress specific in most of the cases; rather it has been placed on top of the specific stress regulation mechanisms in order to combine and coordinate plants’ response under multiple stresses.

14.4.4 Important Genes and/or QTLs Associated with Salt Tolerance and Ion Homeostasis

Genetically, salinity tolerance is a complex quantitative trait (Foolad and Jones 1993) which makes it difficult for plant breeders to select for improved genotypes due to low expressivity, heritability and large effects of environment on the trait. Still, genetic resources are vital for any trait, and intraspecific selection has contributed to improved tolerance in rice (Akbar and Yabuno 1977) and barley (Epstein et al. 1980). Over the past decade, research efforts have focused on the mapping and identification of QTLs contributing to salt stress tolerance through marker-assisted selection (Singh et al. 2007; Haq et al. 2010; Table 14.4). For example, the Saltol QTL in rice was identified by employing a RIL population between the tolerant landrace Pokkali and the highly sensitive IR 29 by AFLP genotyping (Gregorio 1997). Further, it was shown that the Saltol QTL contributed to 43% of variation for seedling shoot Na+/K+ ratio (Bonilla et al. 2002). Lin et al. (2004) identified a total of 11 QTLs from an F2 population including major QTLs for shoot K+ concentration on chromosome 1 (qSKC-1) and shoot Na+ concentration on chromosome 7 (qSNC-7) as derived from a cross between tolerant indica rice (Nona Bokra) and sensitive japonica (Koshihikari). These QTLs were found to influence the root and shoot Na+ and K+ accumulation as well as survival under salt stress. Subsequently, a single QTL, qSKC1 or OsHKT1.5 was fine mapped and successfully cloned (Ren et al. 2005). A list of some of the identified QTLs governing salt stress tolerance in different crop species is provided in Table 14.4, and a list of some experimentally validated gene involved in salt-induced response across plant species is given in Table 14.5. In rice alone, about 70 QTLs for salt stress have been mapped (Hu et al. 2012); however, cloning of QTLs is still a rate-limiting step, mainly due to difficulties in fine mapping and defining precise QTL limits. Hence, there is a need to direct research efforts towards identification of genes governing tolerance to salt stress which in turn would aid in development of perfect gene-based markers and pyramiding of multiple QTLs in a single genetic background so as to provide tolerance under diverse stress environments.

Table 14.4 QTLs governing tolerance to salinity stress in plants
Full size table
Table 14.5 Key gene/gene families involved in governing response to salt stress
Full size table

14.5 Cellular Defence Network and Plant’s Adaptive Strategy

14.5.1 Role of Reactive Oxygen Species (ROS) in Salinity Tolerance

Salt stress disrupts metabolic coordination between different biochemical pathways, leading to formation of high-energy electrons which, when donated to molecular oxygen, result in the formation of different reactive oxygen species (ROS) such as 1O2, H2O2, O2 •− and HO•. The plant organelles, chloroplast, mitochondria and peroxisomes, are the sites of production of ROS in plants; however, detailed biochemical reactions leading to their production are beyond the scope of this chapter. Both ROS formation and associated injury during salt stress in plants have been previously reported (Gomez et al. 2004; Rubio et al. 2009; Chen et al. 2012). ROS-induced damage in plants depends on the nature and severity of stress, the duration of exposure and even environmental conditions. However, it is well known that while ROS accumulation causes intracellular damage to lipids, proteins and DNA (Bi et al. 2009), it also functions as a signalling molecule in plant-pathogen interaction and abiotic stresses (Mittler et al. 2004; Torres and Dangl 2005). The plasma membrane-located NADP oxidase (NOX) genes or the respiratory burst oxidases (RBOH) which catalyse the synthesis of the superoxide radical are important constituents of ROS-mediated signalling system (Desikan et al. 2001; Mittler et al. 2004; Torres and Dangl 2005). Ma et al. (2012) reported that double mutants atrbohD1/F1 and atrbohD2/F2 of Arabidopsis disrupted Na+/K+ homeostasis therefore showing increased sensitivity to NaCl treatments than wild-type or single null mutants. AtrbohF, apart from increasing ROS levels in response to increased soil salinity, also reduced Na+ concentrations in xylem sap and prevented accumulation of excess Na+ in shoot cells through transpiration (Jiang et al. 2012).

Reactive oxygen species (ROS) scavenging is also extremely important for salt tolerance. The main defence against ROS includes enzymes such as ascorbate peroxidase (APX), superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPX), polyphenol oxidase (PPO) and monodehydroascorbate reductase (MDAR) along with low-molecular weight antioxidants such as ascorbate, glutathione, glycine betaine, trehalose, alpha-tocopherol and proline (Foyer and Noctor 2005; Abogadallah 2010). Overexpression of a rice ascorbate peroxidase gene in alfalfa led to improved salt stress tolerance. In rice transgenic overexpressing pea DEAD-box helicase gene PDH45 which also showed improved salt stress tolerance, it was found that the protein PDH45 physically interacts with Cu/Zn SOD, adenosine-5′-phosphosulphate-kinase, cysteine proteinase and eIF(4G) thus implicating the role of ROS-scavenging machinery in stress tolerance (Gill et al. 2013). Transgenic tobacco plants overexpressing cotton type 3 metallothionein gene GhMT3a also showed increased tolerance against different abiotic stresses including salinity stress (Xue et al. 2009). Improved ROS scavenging may also be attained by manipulation of certain master regulator genes. For instance, Schmidt et al. (2013) identified a rice transcription factor, salt-responsive ERF1 (SERF1), that showed increased expression upon salt and H2O2 treatment. SERF1 showed direct binding to promoters of genes like MAPK kinase kinase 6 (MAP3K6), MAPK5, dehydration-responsive element binding 2A (DREB2A) and zinc finger protein 179 (ZFP179) thus suggesting that it may be the master regulator of ROS-activated MAPK cascade during the initial phase of salt stress making way for downstream gene expression changes resulting in salt stress tolerance.

14.5.2 Osmolytes or Compatible Solute-Mediated Adaptation to Salt Stress

Since osmotic imbalance is one of the most prominent effects of salt stress, adaptation to this stress, to a great extent, depends on the ability to mediate quick osmotic adjustment by accumulation of organic osmolytes like proline, mannitol, fructans, trehalose, glycine betaine, ononitol, etc. In fact, due to the importance of osmotic adjustment in salinity stress adaptation and in many other abiotic stresses as well, it has been regarded as the central dogma of stress physiology (Hare et al. 1998). Not many direct evidences, however, confirm this hypothesis, and most of the evidences are largely correlative. Exposed to salt stress, plants start accumulating organic osmolytes, most of which belong to the class of polyhydroxylic compounds (carbohydrates and sugar alcohols) and zwitterionic alkylamines (amino acids and quaternary amines), as an adaptive response. Unlike ROS, which can be potentially damaging to the cell itself, these organic osmolytes are non-toxic in nature and hence are also termed as ‘compatible solutes’. Cumulatively, these compatible solutes decrease the water potential of cell making them osmotically more competent for water uptake. Several reviews are available which discuss about osmolyte accumulation in plant (Bohnert and Jensen 1996; Serrano et al. 1998; Chakraborty et al. 2012b). Given their immense importance, osmolytes have emerged as tempting candidates to engineer stress resistance in crop plants. Several efforts have been made to develop transgenic plants containing osmolyte-synthesizing genes with an ultimate aim to engineer salt and/or drought stress tolerance. Few of such efforts have been successful (Hayashi et al. 1997), while many of them did not (Smart and Flores 1997). Even where some success has been achieved, the improvement was marginal. The limited success of the osmolyte-overexpressing transgenics is not a reason to dismiss their potential in engineering stress adaptation; rather it indicates the fact that the relative proportion of different osmolytes and the spatiotemporal expression of osmolyte-synthesizing genes are more important as compared to the absolute amount (Hare et al. 1998). Untimely, out of place and/or excessive expression of a particular osmolyte can be associated with yield penalty because of metabolite diversion from primary metabolism (which favours growth and yield) to secondary metabolism (which favours defence). Hence, it is imperative that future research needs to focus more on pathway engineering and devising controlled gene regulation machineries to achieve success in this area.

14.6 Possible Management Options for Alleviation of Salinity Stress

Apart from our traditional effort to breed salt-tolerant crop varieties, sometimes improved crop management practices also play important role in counteracting ill effect of salt stress. Hence, we should consider different external management approaches, viz. maintenance of K+ homeostasis and the use of phytohormones for the growing plants in saline environment.

14.6.1 Exogenous Application of Potassium (K+)

Around the world, researchers have attempted to alleviate the salinity stress applying potassium by and large. However, the mode of application varied over the experiments, either by soil or foliar application, while varying doses of sole potassium or in combination with some soil amendments (like FYM) or with external phytohormones. But some of the results obtained during the course of study are indeed exciting and hence addressing to solve the salt stress in crop plants by suitable crop management.

Salt stress is often noticed by the skewed K+/Na+ ratio in actively growing plant tissues along with stunted growth and metabolic activity of plant tissues (Shabala and Cuin 2008; Degl’Innocenti et al. 2009). Excess build-up of tissue Na+ along with reduced uptake and tissue retention of K+ in plant parts has been conspicuous under saline environment (Munns et al. 2002). Several basic physiological processes in plants, like stomatal closure, destruction of chlorophyll pigment system, etc., have been observed to be hampered under salinity (Gama et al. 2009; Parida et al. 2004). The role of K+ is established in regulation of stomatal movement of plant tissue; thus, better maintenance of water storage and cell turgidity can be assured under osmotic stress (Marschner 2012).

Both soil and foliar application of K+ supplemented the growth, yield and fruit quality of tolerant and sensitive cultivars of tomato grown under salinity. It ensured the role of external K+ application apart from genetic tolerance ability to manage the stress (Amjad et al. 2014). Basal application of potassium improved the overall performance of contrasting peanut varieties at defined salinity levels, while TG 37A, the susceptible one, responded better over GG 2, the tolerant one (Chakraborty et al. 2016c). Similarly, Arshadullah et al. (2014) conducted a hydroponic study on sunflower crop and confirmed that 2% K+ foliar application (as K2SO4 solution) revived the tissue K+ concentration after imposition of salt stress, thus resulting in more biomass production.

In other study, Khan et al. (2016) reported that K+ application along with FYM and other nutrients (N, P, Zn) enhanced the growth, yield and fibre quality of cotton plants by reducing the Na+ uptake and Na+/K+ ratio under the salinity. While in most of the cases potassium sources have been restricted to KCl (muriate of potash) or K2SO4 (potassium sulphate) salts, a recent study tested the K2SO4 nanoparticles on growth and physiological responses of forage crop, alfalfa (Medicago sativa L.), under salt stress, and subsequently better performance of nano-fertilizer was revealed by lower electrolyte leakage, higher proline and relative water content, along with higher antioxidant enzyme activities (superoxide dismutase and catalase), and other growth and yield parameters (El-Sharkawy et al. 2017).

14.6.2 Use of Phytohormones

Phytohormones, synonymously used as plant growth regulators, refer to the compounds originated from plant biosynthetic processes that can act either locally (at the site of their synthesis) or transported to some other sites within the plant in order to promote growth and development responses both under normal and adverse/stressful environment (Peleg and Blumwald 2011). A large array of phytohormones like abscisic acid (ABA), gibberellins (GA), ethylene, auxins (IAA), cytokinin (CKs), and brassinosteroids (BRs), has established their role in abiotic stress management (reviewed in Fahad et al. 2015). Moreover, salinity tolerance mechanism via proline biosynthesis as influenced by regulatory role of phytohormones under salinity stress has also been highlighted (reviewed in Iqbal et al. 2014). Kanmani et al. (2017) conducted a pot experiment with contrasting rice varieties (Pokkali and CO51) treated with foliar application of four different plant growth regulators for mitigating the stress. The response of brassinolide (1.0 ppm) was found interesting for photosynthetic rate and chlorophyll fluorescence, and gibberellic acid (50 ppm) increased the chlorophyll content, while enhanced transpiration rate was observed at kinetin application (20 ppm). In other instances, pretreatment with phytohormones (NAA and BAP) in pineapple (cv. MD Gold) minimized the salt stress effects suffered by the plant by maintaining optimum biomass, increasing tissue K+ concentration, reducing the damage to cell membranes and increasing total soluble sugars (Melo et al. 2017).

14.7 Conclusion and Future Research Strategies

Salinity stress is second most important abiotic stress for cultivated crop plants. Salinity-affected area is gradually increasing under the scenario of global climate change. The importance of properly understanding and combating this threat to world agriculture is, therefore, more apprehended by the researchers. Soil salinity adversely affects plant growth and development accompanied by an increase in uptake of Na+ and Cl− ions and a decrease in uptake of K+, Ca2+ and Mg2+ resulting in ionic imbalance, sodium ion injury and disturbed metabolic processes, changed concentration of biomolecules, photosynthetic activity and poor productivity. Other most detrimental effect faced by the plants is sudden outburst of reactive oxygen species produced due to salinity stress, which disrupts the cellular structure and damages subcellular organelles, leading to cell death. At molecular level, efficient operation of different signal proteins and various symporters and antiporters lying either in the plasma membrane or tonoplast plays important role in salinity tolerance. Activity of different Na+/H+ antiporters, viz. SOS1 and NHX1, depends upon the activation of other signal proteins like SOS2, SOS3 and other calcium-binding proteins.

The genotypes having superior antioxidant defence capacity in terms of either accumulation of antioxidants like ascorbic acid, glutathione, malondialdehyde, etc. or higher activity of the enzymes are more capable of withstanding salinity stress. Salinity stress causes osmotic and oxidative stress; hence, genetic modifications in these areas could yield beneficial result in bringing salinity tolerance in crop plants. Incorporation of genes facilitating biosynthesis of compatible solutes whose accumulation will help in osmotic adjustment in the plant cell and thereby maintaining better water balance inside the plant tissues when facing osmotic pressure from outside. Though there is ample opportunity for research in this area, it needs multidisciplinary approaches to address all the component of the problem of salinity.

Adaptation to salinity stress involves osmotic homeostasis, ionic homeostasis, ROS detoxification as well as tissue adaptation mechanisms. These adaptation strategies are governed by a network of several interacting pathways which are controlled by both genetic and epigenetic regulations. In this context, many cultivated accessions were identified with tolerance to salinity stress. QTLs for salt tolerance have been identified from those cultivated accessions. A few of these have been identified, mapped, cloned and introgressed into elite varieties using molecular breeding approaches. Satisfactory progress in transferring tolerance to high-yielding cultivars for better survivability is made. But yield penalty under salinity stress can’t be reduced significantly. In this context, some of the wild relatives with better tolerance are being utilized in breeding. The major setback faced by the breeders in this approach is that most of wild tolerant genotypes are often cross-incompatible with the cultivated species. There is a need to go for mining of the differentially expressed genes and subsequent transfer of those to cultivable species.

The search for novel salt-tolerant genes or protein is presently extended to some of the halophytic plants such as mangroves which can thrive well under extremely saline environment. The successful transfer of the important genes imparting tolerance to soil salinity from mangrove gene pool to some of important crop plants is being attempted. Besides this, mining of the genes is also possible from a wide range of microbial gene pool as well as from Archaea. Apart from the commonly known pathways that impart tolerance to eukaryotes including higher plants, there may be some other mechanisms operating in these organisms which help them to survive in the extreme environment of sea or saline hot spring. During the past few decades, ‘omics’ approaches have opened possibilities of understanding interaction dynamics between genes, proteins, metabolites and small RNA in salinity stress tolerance both under acute and chronic salinity stress. Recent advent of ‘phenomics’ or large-scale phenotyping is expected to further facilitate efficient identification of promising germplasms for enhancing salt stress tolerance. But the progress made so far is still at the infant stage, and mechanisms of salinity tolerance at the morphological, physiological and molecular level are not very well deciphered in all the crops. It is understood that salinity tolerance like other complex abiotic stress tolerance is controlled by many environmentally responsive genes. Many of them are affected by the occasional post-transcriptional modifications due to extreme climatic fluctuation. Under global climate change, ‘envirotyping’ is emerging as a new concept which will predict multiple genes more precisely along with genotyping and phenotyping and haplotypes interacting with environments across developmental stages. This will help in understanding and genetic manipulation for achieving better salinity tolerance. Besides the potential crosstalk of salinity stress regulatory circuit with other pathways governing the overall physiology of the plants is still mostly under cover. Hence, in-depth studies by means of real-time and cutting-edge technologies at cellular and at the whole-plant level is essentially required in the days to come to have a complete understanding for developing salt-tolerant and environment-resilient varieties in the future.