Physiology of Salt Stress in Plants. Группа авторов

minimal ability to increase the ATP production during stress, and increasing salt ions further suppresses the activity of the complex I and complex II of the mtETC (Jacoby et al. 2011). The negative membrane potential of the mitochondrial membrane assisted the intake of Na⁺ to the mitochondria (Che‐Othman et al. 2017), of which excess accumulation inhibits the mtETC by denaturing the proteins of the mtETC complexes or by disassembly of the complexes (Flowers 1972). At the moderate or lower salt stress in glycophytes, the ATP synthase activity increased without affecting different subunits of the ATP synthase. However, the ATP synthase subunits decreased significantly at higher salt stresses (Kosova et al. 2013). Due to presence of alternative mtETC pathways like NAD(P)H‐dehydrogenases, and alternative oxidase (AOX), the ETC is more complex and flexible in mitochondria (Jacoby et al. 2011). Suppression or inhibition of the mtETC negatively impacts the oxidative phosphorylation and ATP production. Moreover, the altered mtETC facilitates the electron's leakage to the free oxygen molecule and produces an excess amount of the ROS. However, the ionic component of the salt stress is more deleterious to the mtETC than the osmotic, affecting the NADH dehydrogenase (complex I) and succinate dehydrogenase (complex II) activity (Hamilton and Heckathorn 2001). Two competing respiratory chains in plant mitochondria help plants maintain the mtETC up to some extent in moderate salt stress. When salt stress inhibits the cytochrome‐mediated respiratory chain activity, the AOX‐mediated chain remains unaffected (Jacoby et al. 2011) and provides metabolic adjustment to the mitochondria at low or moderate salt stress.

      2.4.3 Peroxisome Functioning

Peroxisomes play a crucial role in plant physiology. It is the organelle where β‐oxidation of fatty acids, part of the photorespiratory pathway, glyoxylate cycle, biosynthesis of phytohormones: auxin, JA and SA, and ROS metabolism occurs (Fahy et al. 2017). The peroxisome is the primary site of ROS generation, detoxification, and also involved in energy‐producing metabolism. Hypothetically, it is plausible that in salt stress, the peroxisomes' biogenesis and functional activities might be increased to cope with increased photorespiratory pathway, increased energy demand, and increased ROS level. In several previous studies, the increased number of peroxisomes was reported in plants subjected to salt stress (Mitsuya et al. 2010). A peroxisomal membrane protein family PEX11 is known to regulate the size and number of peroxisome in plants, animals, and yeast (Mitsuya et al. 2010). During salt stress in plants, the expression of proteins from the PEX11 families is upregulated (Fahy et al. 2017; Mitsuya et al. 2010). However, there is no evidence found so far, which supports the hypothesis of increased functional activity of the peroxisome and to understand that a detailed study is still missing.

2.5 Halophytes and Their Physiology

Halophytes are the plant species that can survive and complete their lifecycle in the soil with salinity equivalent or higher than 200 mM of NaCl (Flowers and Colmer 2008). The plasticity of halophytes to tolerate saline soil conditions is attributed to genetic, morphological, anatomical, and physiological adaptations (Flowers et al. 1977). Decades of research accumulated knowledge about the halophytes suggest that they evolved to maintain efficient cellular ion homeostasis, better osmotic adjustments, and secretion of excessive salt by the salt gland or by the epidermal bladder cells (EBC). How halophytes enable them to tolerate the salt stress and differed from the glycophytesis, summarized in Figure 2.1.

Figure 2.1 Schematic illustration shows comparison of ion homeostasis and physiological changes in glycophytes and halophytes during salt stress. The illustration shows only some of the important differences between a glycophyte and a halophyte to provide simplicity of the scheme. The arrows represent the direction of Na⁺ movement during salt stress, whereas the thickness of the arrows indicates the amount of Na⁺ movement. The number of transporters on the membranes represents the amount of Na⁺ being transported to the direction of the arrow. ABA, absiscic acid; CAM, Crassulacean acid metabolism; FV, fast‐activating Na⁺ channel; HKT1, high‐ affinity K⁺‐1 transporter; NHX, vacuolar Na⁺/H⁺ antiporter protein family; SOS1, salt overly sensitive 1 (plasma membrane Na⁺/H⁺ antiporter); SV, slow‐activating Na⁺ channel. Scheme was created using BioRender.com.

      Source: Modified from (Bose et al. 2017; Zhao et al. 2020)

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      2.5.1 Ion Homeostasis in a Halophyte

      The halophytes maintain better cellular ionic homeostasis by efficient Na⁺ exclusion and vacuolar sequestration, xylem loading and retrieval of the Na⁺, minimized recirculation of Na⁺ through the phloem tissue, and secretion of salts through the salt gland and EBCs (Zhao et al. 2020). The constitutively expressing plasma membrane Na⁺/H⁺ antiporter SOS1 in halophytes performs the task of Na⁺ extrusion out of the cell more efficiently than the glycophytes (Shi et al. 2002). The sequestration of the Na⁺ and Cl⁻ in the vacuole of root and leaf cells of halophytes are facilitated by constitutively expressing Na⁺/H⁺ antiporter (NHX), vacuolar H⁺‐inorganic pyrophosphatase (V‐PPase), and vacuolar H⁺‐ATPase (V‐ATPase) (Jha et al. 2011). However, to avoid the leakage of the ions through Na⁺ permeable channels, 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