slow‐ (SV) and fast‐ (FV) activating ion channels, halophytes minimize their activity (Shabala et al. 2020). This efficient sequestration avoids the toxicity of ions on cytoplasmic physiology and also requires less organic osmolytes to adjust the osmotic balance between the cytoplasm and vacuole. The cytoplasm contributes only 10% of the cell volume, and thus halophytes spend relatively very less energy for cytoplasmic osmotic adjustment in comparison with glycophytes in osmolytes biosynthesis (Zhao et al. 2020).
The excess Na+ in the root cortical or parenchyma cell is then loaded to the xylem vessels by NCCS, SOS1, HKT2, or CCC (Ishikawa et al. 2018; Shi et al. 2002) for dilution of the salt ions in the root cells. However, to avoid the ionic imbalance in the photosynthetically active shoot tissues, plants attempt to retrieve back the Na+ from the xylem vessel to the root cells for extrusion. The transporters of HKT1 family retrieve the Na+ from xylem vessel to the root cells and from leaves to the phloem (Munns et al. 2012; van Zelm et al. 2020). Interestingly, the model plant species A. thaliana contains only one gene encoding for the HKT1 in their genome. Whereas, its close halophytic relative E. salsugineum has five genes encoding proteins belonging to the HKT1 family (Wu et al. 2012) suggesting the better Na+ retrieval strategy in the halophytes. However, the anatomical structure of the root very unlikely allows the unloading of the Na+ coming from the shoot tissue through the phloem which remained circulated in the phloem and ultimately creates damage to the young growing tissues and meristematic region (Zhao et al. 2020). The additional checkpoint in halophytes minimizes the damage of the young meristematic tissues by reducing the Na+ retrieval in the phloem tissue. A comparative analysis revealed that barley allows only 10% of the shoot Na+ retrieval to the phloem, whereas in a salinity‐sensitive lupin species, the retrieval rate was 50% of the shoot Na+ concentration (Jeschke et al. 1992). Here then, the question arises, if halophytes are not recirculating their excess Na+ in the shoot through the phloem, then how can they establish the ionic homeostasis in the shoot tissue? The answer to this question emerged from the study on the halophytes, which revealed the development of salt gland or bladder in approximately 50 species of the halophytes (Zhao et al. 2020), playing a role in sequestering the Na+ and Cl− away from the metabolically active cells and secreting them when accumulates in access. These unique structural developments in halophytes with yet unknown mechanisms showed structural and functional variation among themselves. The exo‐recretohalophytes have the salt gland on the leaves’ surface, while the endo‐recretohalophytes collect salt in the vacuole of specialized EBCs (Dassanayake and Larkin 2017).
2.5.2 Osmotic Adjustment
During salt stress, plants have two options for their osmotic adjustments: de‐novo synthesis of organic osmolyte or the uptake of inorganic ions from the soil. Energetically, the former option is costly, whereas the latter option is economic by an order of magnitude to the plants (Munns et al. 2020; Shabala and Shabala 2011), but depends on the plants’ ability to establish an ionic homeostasis during salt stress. At the onset of salt stress, the relative concentration of Na+ in the soil is much higher than the K+ concentration. Thus, the plants are unable to accumulate the most favorable inorganic ion (K+) as an osmolyte. Contrary to the glycophytes, the halophytes adapted to use the Na+ as the cheap osmoticum to maintain cellular turgor pressure, cell elongation, and stomatal operation (Zhao et al. 2020). The halophytes achieved this ability by efficiently sequestering the Na+ and Cl− to the vacuole and organic osmolyte only for the cytosol, which contributes only 10% of the cell volume and thus energetically cheaper to synthesize than the osmolyte for a whole cell (Zhao et al. 2020). Succulence is another necessary morphological adaptation of some of the halophytes from the Chenopodioideae, and Salicornioideae order (Flowers et al. 2015), however, the detailed mechanism of succulence development are not understood yet (Qi et al. 2009). The succulent cells in the halophytes provide them the ability to store the excess Na+ and K+ in those cells, higher H+‐ATPase activity, and nonenzymatic antioxidant activity in this tissue (Zeng et al. 2018; Zhao et al. 2020). Moreover, these succulent cells retain a constitutively lower number of open SV vacuolar channels and suppress the activity of FV in the vacuole.
2.5.3 Physiological and Metabolic Adaptation of Halophytes
Osmotic shock to the plants in salt stress drops the xylem pressure. The guard cells perceive the drop in xylem pressure and different salinity‐induced signaling cascades, to close the stomata with a purpose to minimize water loss. This closure of the stomata or reduction in the stomatal conductance poses a penalty on the plants by reduced CO2 assimilation and decreased growth rate of the plants. The stomatal density and the stomatal aperture size regulate the gaseous exchange through the stomata. The halophytes adapted themselves efficiently to control the stomatal aperture and the stomatal density in salt stress with a minimal negative impact on photosynthesis (Zhao et al. 2020). The level of ABA content in the xylem sap and leaves were maintained much lower in halophytes in comparison with the glycophytes (Hedrich and Shabala 2018). More strikingly, the halophyte guard cells have a different sensitivity to the ROS produced during the salt stress, and the Na+ regulates the opening and closing of the stomatal aperture in halophytes contrary to the K+ in the glycophytes (Chiang et al. 2016). This adaptation provides advantages to the halophytes over glycophytes in maintaining the better gas exchange and the efficient photosynthetic ability to the halophytes in saline soil condition. Halophytes change the architecture of the photosynthetic complexes by omitting the salt‐stress‐sensitive component from the complexes and avoid the ROS‐induced photoinhibition of PSII and PSI (Pagliano et al. 2009; Trotta et al. 2012). For maintaining ROS homeostasis during photosynthesis, halophytes use Na+ accumulated in the chloroplast, for the exchange of ascorbate, pyruvate, and phosphate to the chloroplast through different Na+ transporters on the chloroplast membrane (Bose et al. 2017). The activity of the enzymes involved in the Calvin–Benson–Bassham cycle could be highly sensitive to the change of the ionic balance and availability in the chloroplast during the salt stress. This example comes from the enzyme FBPase of rice whose in vitro activity was suppressed at very low concentration of the NaCl, whereas the same enzyme from a close halophytic relative of rice, Porteresia coarctata, showed very less inhibition on its activity. The sequence analysis of P. coarctata from rice and P. coarctata exhibited a mutation of a few amino acids in PcFBPase, which resulted in reduced sensitivity of the enzyme to the salt stress (Ghosh et al. 2001).
2.6 Halophytes in Agriculture and Land Management
Approximately, 90% of the cultivated crops are sensitive to salt stress (Zörb et al. 2019), and thus for the irrigation of these crops, freshwater is used extensively. An estimation revealed that 70% of all available freshwater is used for irrigation at the global level. In comparison, in developing countries, the statistics reach 90% (Panta et al. 2016). Thus, the use of crop species with better water‐use efficiency may provide an alternative to this adversary and save freshwater resources. However, with the increasing trend of the soil salinization either due to the natural cause or due to the anthropogenic activity, this approach seems to be less realistic. In the past decade, several research articles were published to provide information about the improved salt‐stress tolerance in different crops under the lab conditions. However, due to the social concern and strict regulatory processes, only a few have been tested in the field conditions. The fact is that transferring only one salt‐stress responsive gene in a crop is not sufficient to improve the salt‐stress tolerance in the crop plants under the field conditions. Instead, it may be possible by pyramiding of several regulatory and stress‐tolerance genes, which may require several years of research and economic costs. The better alternative strategy would be to use the halophytic plant species in the land degraded by salinity and use of the saline water for the irrigation of these plants. There is no limitation of the saline water coming either from the sea or as the industrial wastewater. This strategy provides no competition for the available freshwater, and the wasteland will be recycled.
