Introduction

Soil salinity is a severe challenge affecting agricultural productivity globally. Declining cultivable lands due to soil salinization and the increase in food demand due to the population surge further worsen the situation (Kumar and Sharma 2020). Hence, there is an urgent need to deal with the soil salinity problem in the agricultural sector. Cultivation of salt-tolerant crop varieties in saline lands could be a potential solution to recover the soil quality and sustainable agricultural production (Kumar and Sharma 2020). Na+ is one of the predominant ions responsible for salinity. Because excess Na+ interferes with the regular metabolic activity in plants, the Na+ level is maintained lower than the K+ level in plant cytoplasm.

A simplified scheme of salinity stress in the plant is presented in Fig. 1. The entire processes of perception, signaling, and response to the salinity stress can be outlined as follows. The osmosensory and ion-sensory proteins in the cell wall and the plasma membrane perceive salinity in the form of osmotic and ionic stress, respectively. Osmotic and ionic stress results in the intracellular Ca2+ spike, acting as a signal, initiating several downstream processes such as plasma membrane enzyme-dependent Reactive Oxygen Species (ROS) production. ROS production causes oxidative stress. In response to the signaling and oxidative stress, membrane transporters and pumps get involved in reducing the salinity stress. The recovery from salinity stress is caused by Na+ extrusion, Na+ compartmentalization, and partitioning of Na+ across the plant organs (Van Zelm et al. 2020). Further, the small molecule transporters also transport the phytohormones and compatible solutes during the recovery phase. Hence membrane proteins (Table 1.) can be regarded as a checkpoint of the pathways that requires connecting external stimuli to the intracellular repercussion.

Fig. 1
figure 1

Simplified scheme of salinity stress in plants: plants perceive salinity as osmotic and ionic stress and is consequently converted into Ca2+ signaling. Ca2+ also activates apoplastic ROS production through plasma membrane RBoH enzyme. Plant aquaporin transports ROS into the cytosol, facilitating oxidative stress. Ca2+ and ROS act as long-distance stress signal that activates many pathways to mitigate salinity stress. The main job of the signaling is to activate proteins and different transcription factor-mediated gene expressions primarily involved in Na+ extrusion, Na+ compartmentalization, Na+ distribution, cell damage repair, osmotic balance, and metabolism

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Table 1 Membrane proteins involved in plant salinity stress
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Recent genomic data of different plant species suggested that many membrane proteins in the plant genome are involved in abiotic stress tolerance (Tang et al. 2020). Despite a large number of membrane proteins in plant salinity stress, they can be categorized into a few basic types based on their primary function: ion homeostasis, osmosensing or ion sensing, signaling, redox homeostasis, solute transport, and accessory membrane polypeptides and proteins. In this work, a comprehensive review of plant membrane proteins in salinity stress is done. The review also discusses the role of solute transporters and accessory proteins in plant salt tolerance. Finally, the knowledge gap in membrane proteins in plant salinity stress response and the possibilities to develop salt-tolerant crops based on the plant membrane protein are discussed.

Membrane Proteins in Ion Homeostasis

Membrane Proteins in Sodium Homeostasis

Na+ stress in plants is primarily sensed and controlled by the roots. No Na+ specific channels on plant root plasma membrane are identified to date. A recent proposition suggests that vesicular transport enables a large Na+ influx into halophyte cells (Flowers et al. 2019). However, several non-selective cation channels (NSCC) are also believed to be involved in the initial Na+ influx (Demidchik and Maathuis 2007) (Fig. 2). High Affinity K+ Transporters (HKTs) are one group of non-selective ion channel/transporter that transport Na+ and K+ (Riedelsberger et al. 2021). Several HKT genes and their functions in plants are highly variable, but their primary functions are ion accumulation under starved conditions, salt tolerance by ion compartmentalization, and partitioning (Hamamoto et al. 2015). Class I HKT channels are evidenced to perform K+ and Na+ transport (Gassmann et al. 1996). Overexpression of HKT1 has promoted salt tolerance by locally restricting Na+ (Wang et al. 2019a). Class II HKTs co-transport Na+ and K+ and are activated during K+ deficiency. One of the members of class II, HKT2;1, is responsible for distributing the Na+ from root to shoot, thereby enhancing the salt tolerance in barley (Mian et al. 2011). HKT2;1 is also responsible for increasing Na+ content in plant cell. Excess Na+ is toxic; hence repression of HKT2;1 gene is also demonstrated to improve salt tolerance in rice (Wei et al. 2021). Na+ is also transported through the High-Affinity K+ uptake (HAK) family of transporters. For example, a HAK family transporter ZmHAK24 in maize and its orthologues in rice and wheat specifically transport Na+; confer salt tolerance by restricting Na+ in the root (Zhang et al. 2019). HAK activity is more relevant to the K+ acquisition; therefore will be discussed in the K+ homeostasis section. Na+ homeostasis is also controlled by the ligand-gated channels such as Cyclic Nucleotide Gated Channels (CNGCs) (Jarratt-Barnham et al. 2021). Expression profiles of CNGCs change with salt stress. A CNGC homolog in Arabidopsis thaliana AtCNGC10 contributes to the increase in [Na+]cytosol under saline environmental conditions hence it negatively regulates plant salt tolerance (Jin et al. 2015). Another group of ligand-gated ion channels, ionotropic glutamate receptors channels (iGluRs), are also implicated in transporting Na+ and K+. The precise role of iGluRs in maintaining the K+/Na+ ratio is not clear but it has been regarded as one of the means to tackle salinity stress (Demidchik et al. 2004).

Fig. 2
figure 2

Ion and solute transporting membrane proteins: Plasma membrane (pm) and intracellular membrane transporters (in) are shown. The primary function of each type of transporter is numbered, and corresponding descriptions are enlisted. Plasma membrane (pm) transporters are mainly responsible for the ion extrusion and distribution across different plant organs, whereas intracellular (in) transporters do the compartmentalization and locally control the ion concentration. Non-selective ion channels do not discriminate between Na+ and K+ and can be non-gated or ligand-gated. K+ specific channels are mainly voltage-gated. Intracellular Ca2+-ATPase participates in Ca2+ homeostasis. Many solute transporters are driven by ions, whereas ABC transporters are driven by ATP hydrolysis

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Na+ transport by secondary active transporters mainly occurs during the recovery phase. The primary Na+ extruding plant plasma membrane secondary active transporter is SOS1 (NHX7 in Arabidopsis) (Wu et al. 1996). It is a Na+/H+ antiporter that transports Na+ out of the cytosol in exchange for H+. SOS1 is also vital for the root-to-shoot distribution of Na+ in plants, thus conferring a long-distance salt transport (Shi et al. 2002). Plant intracellular Na+/H+ antiporters NHXs also play a significant role in salt tolerance. (Apse et al. 1999; Bassil et al. 2019). NHXs are involved in Na+ compartmentalization, but their activity can vary from one plant to the other depending on the level of salt tolerance (Rodríguez-Rosales et al. 2009). In Arabidopsis, NHX1 and NHX2 can transport Na+ and K+, but when the cytoplasmic Na+ concentration increases, the transporters participate in the sequestration of Na+ in the vacuole; hence contribute to the plant salt tolerance (Bassil et al. 2019). NHX5 and NHX6 reside in the endosomal membrane to confer protein sorting during salt stress (Bassil et al. 2019). The other two NHXs of Arabidopsis, NHX3, and NHX4, are more specific toward Na+ and K+, respectively, and are mainly involved in vacuole transport and pH maintenance (Bassil et al. 2019). The functioning of Na+/H+ antiporter is driven by the proton gradient, which is established by H+-ATPases and H+-PPases (Shi et al. 2002; Silva and Gerós 2009). The fact that the deletion of plasma membrane H+-ATPase becomes salt sensitive and the overexpression of the same with SOS1 increases salinity tolerance in Arabidopsis endorse the importance of plasma membrane-H+-ATPase (Fan et al. 2019). Unlike Arabidopsis, the expression profile and the regulation of plasma membrane H+-ATPase activity of the salt-resistant plant is different. The comparison showed that ATPase activity increases upon salt exposure in leaves of salt-tolerant plants compared to salt-sensitive plants (Sahu and Shaw 2009). Further analysis showed that the variability of the H+-ATPase activity could be due to the different regulatory networks present in these plants (Gévaudant et al. 2007). Vacuolar-H+-ATPase (VHA) and H+-pyrophosphatase (H+-PPase) present in tonoplast energize the NHXs to compartmentalize salts in tonoplast (Kluge et al. 2003). Like plasma membrane H+-ATPase, VHA also shows an altered expression profile and activity level in salt-tolerant plants compared to a salt-sensitive plants (Wang et al. 2001; Jaarsma and De Boer 2018). However, research showed that VHA is essential for nutrient storage in tonoplast, whereas H+-PPase creates the H+ gradient for salt accumulation (Krebs et al. 2010).

Membrane Proteins in Potassium Homeostasis

Like Na+, K+ absorption and distribution are essential to maintain the K+/Na+ ratio. K+ channels (Fig. 2) responsible for plant salt tolerance are primarily voltage-gated channels and belong to three major groups: inward rectifying—controlling K+ influx (AKT1, KAT1), outward rectifying—controlling K+ efflux (SKOR and GORK), and weakly voltage regulated—direct both in and out K+ transport (AKT2 and AKT3) (Shabala and Cuin 2008; Dreyer and Uozumi 2011). These channels are also regarded as shaker-type K+ channels. The major inward rectifying K+ channels found to enhance salt tolerance are KAT1 and AKT1. KAT1 is shown to increase salt tolerance in yeast. KAT1 increases the K+ content in cells upon salinity stress (Obata et al. 2007). AKT1, on the other hand, is responsible for K+ uptake and drought tolerance (Ahmad et al. 2016b). Outward rectifying channels such as GORK response to the salinity stress induced depolarization of the plasma membrane. Depolarization occurs due to the increasing Na+ influx into the cell. In response to the depolarization, GORK maintain the plasma membrane potential by removal of cellular K+. This destabilizes the cytosolic K+/Na+ ratio. Therefore, to prevent depolarization-mediated K+ loss, plant reduces the expression of GORK (Adem et al. 2020). Another K+ channel of the same group, Stelar K+ Outward Rectifier (SKOR), passes the K+ to the xylem for its distribution. It is demonstrated that a constitutive expression of melon SKOR in Arabidopsis improves its salinity tolerance (Long-Tang et al. 2018). Outward rectifying K+ channels are also crucial for long-distance K+ transport, balancing the cytosolic K+/Na+ ratio (Wegner and De Boer 1997). The weakly voltage-regulated K+ channels AKT2/AKT3 demonstrated that the direction of the rectification and the voltage dependency is due to the sequence variations among different plants (Huang et al. 2021). AKT2/AKT3 control K+ content and hence sucrose transport in phloem cells (Rubio et al. 2020). In rice, AKT2/AKT3 expression levels are reduced during salinity stress; however, its impotence may vary in plants depending on the variations in the direction of the rectification and the voltage dependency.

(Schmidt et al. 2013; Huang et al. 2021). Non-voltage gated K+ channels in plants are two-pore channels (TPC) that are exclusively located in the tonoplast or intracellular membrane. The primary function of the K+ specific TPC is to transport K+ toward the cytoplasmic direction to stabilize the cytoplasm K+/Na+ ratio. Overexpression of K+ specific TPC is therefore expected to resist the salt stress. Transgenic overexpression of TPCs improves plant salt tolerance (Wang et al. 2013; Ahmad et al. 2016a). Recently a structure-based study of Arabidopsis two-pore channel AtTPC1 shows that the channel is specific to Ca2+ but cannot discriminate between monovalent ions (Na+ and K+) (Guo et al. 2017).

Transporter and carrier protein entailing K+ transport across plant membrane belongs to KT/HAK/KUP transporter family (Li et al. 2018). HAK transporters are comparatively well-characterized members of the KT/HAK/KUP transporter family. Although the variation of ion specificity has been reported for HAK members in plants, HAK transporters preferably transport K+. Depending on the expression and localization, it primarily renders a K+ accumulation in the plant during low K+ environments and maintains the K+/Na+ ratio by redistributing K+ (Nieves-Cordones et al. 2010; Shen et al. 2015).

Cation/H+ antiporters are a large group of secondary active transporters in plants and can be subdivided into three main types: NHX, CHX, and KEA (Chanroj et al. 2012; Jia et al. 2018). Their functions and physiological roles are diverse (Isayenkov et al. 2020; Tsujii et al. 2020). While most NHXs preferentially transport Na+, quite a few K+ transporting CHXs are known. AtCHX13 and AtCHX14 are two critical Arabidopsis transporters active during K+ deficiency in the environment. AtCHX13 is located in the root carrying out the acquisition of K+, whereas AtCHX14 is expressed in the xylem parenchyma cell controlling the root to shoot movement of K+ (Zhao et al. 2015). A cation/H+ antiporter GsCHX19.3 of Glycine soja shows a relatively higher expression in leaf and flower in response to the salinity stress (Jia et al. 2017). GsCHX19.3 shows the highest homology with A. thaliana CHX19, and when overexpressed in Arabidopsis, it confers salt tolerance. The primary roles of K+/H+ transporters are restricting K+ outflow from root cells and distributing K+ from root to shoot.

Membrane Proteins in Chloride and Nitrogen Homeostasis

Chlorine and nitrogen are two elements absorbed and transported in plants as anions. Chloride homeostasis plays a significant part in plant salinity tolerance. In some plants, such as soybean and avocado, Cl− shows a more toxic effect than Na+ because these plants have a robust Na+ exclusion system than Cl− (Wu and Li 2019). Chloride transporters (Fig. 2) such as Slow Anion Channels (SLAC/SLAH) and Chloride channels (CLC) are documented to affect salt tolerance directly. In Arabidopsis, AtSLAH is critical in Cl− homeostasis during salinity stress. AtSLAH1 and AtSLAH3 heteromer has a significant contribution to the chloride distribution from root to shoot under salinity stress. During salinity stress, reduced AtSLAH1 expression causes decline in Cl− content in xylem sap; preventing Cl− from reaching the shoot (Cubero-Font et al. 2016; Qiu et al. 2016). Other chloride channels such as CLCs are intracellular and perform variable functions. AtCLCc and AtCLCg are two important chloride transporters responsible for salinity tolerance in Arabidopsis (Nguyen et al. 2016). The primary function of AtCLCg is to reduce the shoot Cl− content by compartmentalizing in the parenchyma cell. Cl− exclusion from shoot to root has been widely studied in legume plants (Teakle and Tyerman 2010). Legume plants are unique due to their symbiotic relationship and can better manage chloride and nitrogen distribution (Vincill et al. 2005). For example, the genome-wide association study (GWAS) in soybean revealed that the chloride transporter GsCLC-c2 has significant role in salinity tolerance in soybean (Wei et al. 2019; Luo et al. 2021). In principle, plant chloride channels restrict the distribution of Cl− by compartmentalization.

Nitrogen in the form of NO3− is transported during salinity stress and is often correlated with K+ transport (Raddatz et al. 2020). Nitrate transport is partly achieved by anion (chloride) channels SLAC/SLAH and CLC. The other two nitrate transporters, NTR1 and NTR2, are H+-coupled NO3− symporters native to the plasma membrane. NTR1 and NTR2 are suggested to work due to the H+ gradient established by plasma membrane H+-ATPase (Liu et al. 2021). NRT1 and NRT2, both groups of nitrate transporters, are shown to be upregulated under salinity stress (Wang et al. 2012a; Liu et al. 2021). The NRT group of NO3− transporters mainly performs nitrogen absorption and distribution.

Membrane Protein in Calcium Homeostasis

Calcium ion transport systems can be subdivided into the Ca2+ influx and the Ca2+ efflux (Fig. 2) (Demidchik et al. 2018). Perception of salinity stress transiently induces Ca2+ influx into the cytosol, further amplified by ROS signaling, and is fundamentally required for propagating long-distance salinity stress signals (Choi et al. 2014). The efflux system is essential to move Ca2+ into the subcellular organelle, as a high concentration of Ca2+ in cytoplasm is toxic. The influx system consists of mechanosensitive channels (OSCA), cyclic nucleotide-gated channels (CNGC), two-pore channels (TPC), and ionotropic glutamate receptor channels (iGluRs) essential for an early stage of salinity stress perception. Mechanosensitive Ca2+ channels OSCA in plants sense the osmotic stress and are activated by the mechanical tension in the membrane (Hou et al. 2014; Yuan et al. 2014) (Fig. 3). Transgenic expression of rice OsOSCA1.4 in A. thaliana OSCA1.1 mutant can complement salinity and osmotic stress response (Zhai et al. 2020). Cyclic nucleotide-gated channels (CNGCs) are the ligand-gated channels with an assigned role in various stress tolerances (Demidchik et al. 2018). Most CNGCs are non-selective cation channels, but A. thaliana CNGC10 has been elucidated to have a role in salt tolerance. AtCNGC10 is critical in balancing the K+/Na+ ratio; nevertheless, its inactivation to increase the root K+/Na+ ratio corroborates that AtCNGC10 negatively regulates salt tolerance (Guo et al. 2008; Jin et al. 2015). Since CNGCs require cyclic nucleotide for their activation, it is possible that AtCNGC10 functions downstream to a membrane-associated osmosensory protein that produces cGMP. Similar activation has been reported for AtCNGC2, induced by the receptor-like kinase AtPepR1 producing cGMP (Qi et al. 2010). Two-pore channels (TPC) are responsible for propagating long-distance Ca2+-dependent salinity stress signals (Choi et al. 2014). A study on the A. thaliana two-pore channel shows that AtTPC1 is specific to Ca2+ but less specific to Na+ and K+ (Guo et al. 2017).

Fig. 3
figure 3

Three basic modes of salinity stress perception in plants: Osmotic stress realized by putative osmosensor induces membrane tension. Membrane tension activates mechanosensitive Ca2 + channels. Another mechanism involving plasma membrane protein MOCA1 synthesizes glycosphingolipids in response to the Na+ ion stress. MOCA1 possibly works via changing the plasma membrane dynamics to activate a putative Ca2+ channel. A third mechanism depends on the plasma membrane receptor-like kinases (RLKs) that detect damage to the cell wall or are activated by external stimuli such as ROS. RLKs directly or indirectly activate Ca2+ channels initiating the Ca2+ signal

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Unlike Ca2+ influx into the cytosol, its efflux is energy-dependent. The primary contributor to this relatively slow process is the endomembrane localized Ca2+-ATPase. Arabidopsis ACA2 and ACA4 are two plant endomembrane Ca2+-ATPases whose transcript levels increase during salt stress (Geisler et al. 2000; Anil et al. 2008). Expressing ACA2 in Ca2+-ATPase-devoid yeast cells shows a rapid decrease in cytosolic Ca2+ upon salt stress (Anil et al. 2008). Plasma membrane Ca2+-ATPases from other plants have been demonstrated to function in salt tolerance, as evidenced by the increased transcript levels during salinity stress (Huda et al. 2013). Other contributors to the cytoplasmic Ca2+ restoration are secondary active transporters such as Ca2+/cation antiporters. Plant Ca2+/cation exchangers are predominantly localized in the vacuole and have been examined for their function in yeasts. Ca2+/H+ exchanger CAX1 of A. thaliana is expressed in mesophyll cells and required for Ca2+ storage in the vacuole (Conn et al. 2011). Salinity stress enhances the expression level of both CAX1 and VHA, corroborating that CAX1 activity is energized by vacuolar H+-ATPase (Han et al. 2011). Some Ca2+ exchangers couple Ca2+ transport with Na+ transport. For instance, A. thaliana AtNCL, a vacuolar Ca2+/Na+ exchanger sequesters Ca2+ into vacuole and releases Na+ into cytosol. Therefore, unlike CAX, AtNCL negatively influences salt tolerance (Wang et al. 2012b).

Membrane Proteins in Salinity Stress Signal Transduction

Changes in osmotic pressure and ionic concentration are two factors detected by plants to realize salinity stress (Fig. 3). Osmotic pressure causes several changes to the cellular structures of root cells, inflicting cell wall damage and an osmotic imbalance across the cell membrane. Osmosensors located in the plasma membrane can induce tension in the membrane (Haswell and Verslues 2015). Currently, the osmosensors in plants those induce membrane tension in response to salinity stress are not known (Wang et al. 2022). However, the osmosensing could be due to multiple factors. One predominant factor is the direct distortion of the plasma membrane, inducing membrane tension. Mechanosensing Ca2+ channel protein families such as OSCA are activated due to the plasma membrane tension and initiate Ca2+ signaling (Yuan et al. 2014). Other mechanosensing membrane proteins are predicted to convert the osmotic stress into cGMP formation (Julkowska and Testerink 2015). Cyclic GMP is responsible for activating multiple non-selective ion channels including putative Ca2+ channels (Turek and Irving 2021). Na+ sensors are also elucidated in plants. Monocation-Induced [Ca2+]intracellular Increases 1 (MOCA1) is one such protein that mediates sensing of extracellular Na+ concentration and Ca2+ signaling (Jiang et al. 2019). MOCA1 is a membrane protein with glucuronosyltransferase activity and is responsible for glycosphingolipid synthesis. The exact mechanism of MOCA1 is unknown, but it is thought to be responsible for nanodomain formation in plasma membrane. Nanodomain causes the activation of putative Ca2+ channels (Steinhorst and Kudla 2019).

Receptor-like kinases (RLKs) are integral membrane or membrane-associated proteins involved in various functions, including biotic and abiotic stress perception (Dievart et al. 2020) (Fig. 3). The basic structure of these proteins is composed of a sensory domain, followed by a transmembrane domain and the cytoplasmic kinase domain (Jose et al. 2020). However, some RLKs might have an extension to the cell wall, and some RLKs are only cytoplasmic (Jose et al. 2020). The kinase domain is responsible for phosphorylating a target protein for signal transduction. RLKs directly sense the osmotic damage of the cell wall or oxidative damage of the cell membrane induced by the salinity stress (Ye et al. 2017). RLKs can be root or shoot specific, and their expressions can be up or down-regulated by the salinity stress. For instance, the LRR (Leucine-Rich Repeat)-type RLK, LP2 overexpression in rice is predominantly found in leaves, reducing salt tolerance (Wu et al. 2015). Many RLKs are induced by ROS levels and aim to control the ROS-mediated damage during salinity stress. For instance, the rice RLKs, OsSlk1, and OsSTLK are induced by salt stress and reduce the ROS load and lipid oxidation (Ouyang et al. 2010; Lin et al. 2020). Some RLKs spanning the cell wall recognize peptide hormones expressed due to salinity stress. For instance, overexpression of the small hormone-like peptide AtPep3 is the consequence of salinity stress. AtPep3 interacts through Peptide Receptor 1 (PepR1), a RLK proposed to confer salt tolerance via ion homeostasis (Nakaminami et al. 2018). Salt stress resulting in damage in the cell wall and cell–cell interaction is sensed by RLK named FERONIA, which was also proposed to work toward Ca2+ ion homeostasis (Feng et al. 2018). FERONIA is linked to the cell wall residing Leucine–Rich Repeat Extensions (LRX) domain that senses the cell wall damage (Zhao et al. 2018). Receptor-like kinases might have a link with the plant G-proteins. G-proteins (Ga and Gb) are also upregulated in response to the increase in salinity stress. It is an enigma if G-proteins interact with the limited number of G-protein coupled receptors present in the plant (Misra et al. 2007). However, it is proposed that the G-proteins might just work through RLK signaling (Pandey 2020).

Membrane Proteins for Reactive Oxygen Species Scavenging System

Reactive oxygen species (ROS) generated in roots play a critical role in plants sensing salinity stress. ROS travel from root to shoot results in several changes in shoot, such as the closing of the guard cells (Choi et al. 2014). A coordinated movement of ROS and Ca2+ from root to shoot is also responsible for stress signaling (Li et al. 2021). Salinity stress-related ROS is produced by the plant plasma membrane Respiratory Burst Oxidase Homolog (RBoH). Among the ten RBoHs in Arabidopsis, RBoHD and RBoHF are two extensively studied enzymes directly involved in salinity stress (Ma et al. 2012). Activation of RBoH is the downstream effect of the early calcium influx into the cytosol, where the Ca2+ binding CBL sensors (Calcineurin B-like calcium sensors) and protein kinase (CIPK) synergistically activate RBoHs (Ogasawara et al. 2008; Drerup et al. 2013). RBoHs produce ROS in the apoplastic region to minimize the negative effect of ROS in the cytosol. However, apoplastic ROS is critical for the activities of the plasma membrane pumps and voltage-gated ion channels. One known example is the regulation of the voltage-gated K+ channel SKOR. A cysteine residue located at the apoplastic side of SKOR undergoes ROS-dependent modification to kick-start the K+ transport (Garcia-Mata et al. 2010). Another target of apoplastic ROS is HPCA1, which is a receptor-like kinase. Apoplastic ROS oxidized an extracellular cysteine residue of HPCA1 that activates the protein and relays a putative Ca2+ channel opening in guard cells (Wu et al. 2020).

ROS entry to the cytosol occurs via the PLASMAMEMBRANE INTRINSIC PROTEINS (PIPs) or aquaporins (Dynowski et al. 2008) (Fig. 1). ROS molecules such as hydrogen peroxidase (H2O2) impose oxidative stress by damaging the membrane lipids, DNA, proteins, perturbing the cytosolic redox potential, and positively influencing Ca2+ signaling (Seifikalhor et al. 2019). A common outcome of salinity stress is the change in ROS-mediated membrane permeability caused by lipid peroxidation (Mansour 2013). Another adverse effect of ROS is the activation of the IAA pathway, which leads to root growth cessation (Huang et al. 2019a). Plants discharge multiple antioxidative defense enzymes and compatible solutes to counter oxidative stress (Apel and Hirt 2004). Studying the salinity tolerance mechanisms in halophytes revealed that the better salt-tolerant plant could better manage oxidative stress (Kumar et al. 2021). Membrane proteins also take part in ROS homeostasis. Arabidopsis mitochondrial voltage-dependent anion channel (VDAC) manifests salt tolerance by ROS homeostasis (Sanyal et al. 2020). ROS positively contributes to sensing and preventing salt tolerance through Ca2+ signaling. Data suggests that ROS indirectly activates the intracellular K+ channel, TPC1, for cytosolic Ca2+ spike and, together, they are responsible for the propagation of the salinity stress signal and prevention (Evans et al. 2016). Another instance that ROS contributes to the increase in salt tolerance could be comprehended by ROS regulation of plant annexins. Annexins are the Ca2+ binding membrane-associated proteins responsible for intracellular Ca2+ transport. Arabidopsis Annexins, AtANN1, and AtANN4 negatively regulate salt tolerance (Huh et al. 2010). AtANN1 is again negatively regulated by ROS, implicating that ROS has some positive affects in salt tolerance (Richards et al. 2014). Regulation of membrane protein expression by ROS is also demonstrated. Transcriptome analyses of differentially expressed genes in pumpkin reveal that ROS-producing RBoHD controls the expression of plasma membrane H+-ATPase (AHA1) and the K+ channel HAK5 contributing to the salt tolerance (Huang et al. 2019b). Pumpkin-grafted cucumber plants with inhibited ROS production show compromised salt tolerance and reduced plasma membrane H+-ATPase activity (Niu et al. 2018). These results imply that ROS contributes to salt tolerance by sounding the alarm of salinity-induced damage to the cells and regulating the membrane transporters' activities.

Solute Transporters

Salinity stress induces the expression level of certain solute transporters delineating their importance in salt tolerance. Solute transporters (Fig. 2) are generally involved during the recovery phase and transport three basic groups of molecules: phytohormones, compatible solutes, and metabolites. Phytohormones are essential for signaling growth and development. ABC (ATP Binding Cassette) transporters are primarily involved in phytohormone transport (Fig. 2). For example, Abscisic acids are considered stress response hormones transported by ABCG25, which expression level changes due to the salinity stress (Park et al. 2016). An Arabidopsis ABC transporter, AtABCG36, is suggested to transport phytohormones with a putative role in salt tolerance (Kim et al. 2010).

Compatible solutes or osmoticum transport is imminent during osmotic shock. Molecules such as proline, polyamines, and glycinebetaine reduce oxidative stress and provide osmoprotection under salinity stress; hence called compatible solutes or osmoticum. Only a handful of compatible solute transporters are currently attributed to the plant's salinity stress response. Proline transporter ProT2 is one such membrane protein. ProT2 expression level coincides with the proline accumulation level in the leaves. ProT2 upregulation is the consequence of salinity stress that ensures the long-distance transport of proline (Rentsch et al. 1996). Polyamine is another compatible solute that is overproduced in response to salinity stress. The recent evidence of polyamine transporter PUT3 physically interacting with Na+/H+ antiporter SOS1 in plasma membrane shows a possibility of PUT3 involvement in salt tolerance (Chai et al. 2020).

A significant amount of energy is invested in the recovery phase of salt-induced damage. Therefore, metabolite transporters are essential that keep up the supplies of sugars and other molecules. Numerous studies have identified the change in plant metabolite transporters' expression profiles during salinity stress (Hsu et al. 2009). Sugar transporters STP13 and UPS5 are shown differential activation pattern during salt-stressed conditions. STP13 in Arabidopsis root increases carbohydrate absorption activity of root cells during stressed conditions (Yamada et al. 2011). Ureide permease 5 (UPS5) in Arabidopsis confers salt tolerance by distributing the small molecule allantoin (Lescano et al. 2016). Additionally, UPS5 exhibits salt tolerance by root-to-shoot transport of allantoin, a metabolite pertinent to abiotic stress. Plant cell wall and cell membrane synthesis required a considerable investment of energy. A phosphate transporter PHT4;6 is essential for recycling phosphate from glycosylation toward the synthesis of cell walls and membranes (Cubero et al. 2009).

Accessory Membrane Polypeptides and Proteins

Numerous studies have identified the role of integral membrane polypeptides and proteins in plant salt tolerance. The primary roles of these proteins are yet to be identified. However, these proteins may be responsible for the stability, activity, and targeting of membrane transporters or specific ions. A group of small transmembrane polypeptides called RCI (Rare Cold Inducible) are identified in plants contributing to salt tolerance. RCI polypeptides share significant homology with the yeast PMP3 (Plasma Membrane Protein 3) peptide, which, when deleted, exhibits a salt-sensitive phenotype (Navarre and Goffeau 2000). Overexpression of RCI2A in A. thaliana increases salt tolerance by reducing the cellular Na+ content (Mitsuya et al. 2005). The transgenic expression of Musa paradisica RCI gene in A. thaliana RCI2 mutant recovered Na+ tolerance (Liu et al. 2012). It has been predicted that RCI enhances Na+ tolerance by reducing Na+ content in the shoot, maintaining plasma membrane fluidity, and increasing plasma membrane H+-ATPase activity. A different group of plasma membrane polypeptide SALP1 is identified in rice that also functions to reduce Na+ content in the shoot. In addition, SALP1 increases the proline content in rice (Yuan et al. 2016). The third group of membrane polypeptides, called ABA-induced wheat plasma membrane polypeptide 19 (AWPM-19) is also linked to the salt stress in plants. OsPM1, an AWPM-19, has a proven role in ABA signaling and involvement in stress tolerance (Yao et al. 2018). However, it has been recently demonstrated that OsPM1 has a positive role in drought tolerance but a negative role in salinity tolerance (Wang et al. 2021). Some accessory integral membrane proteins are also evidenced in interacting with the ion transporters. For example, Patellin-1, a membrane trafficking protein, interacts with SOS1 Na+/H+ antiporter to negatively regulate its activity (Zhou et al. 2018). Another membrane trafficking salt-responsive protein, Flotillin-2, potentially interacts with plasma membrane H+-ATPase as detected in mass spectrometry analysis (Junková et al. 2018). Flotillins are also predicted to do intracellular trafficking of Na+ and are associated with plant salt stress tolerance (Flowers et al. 2019; Khalilova et al. 2020). Remorins are another group of accessory membrane protein usually found in microdomains (Raffaele et al. 2009). When transiently overexpressed in Arabidopsis, the Remorin gene SiREM6 of Setaria italic enhances salt tolerance (Yue et al. 2014). However, the precise functions of the accessory integral membrane proteins are not known.

Future Directions

Membrane proteins play an essential role in plant salinity stress. Particularly, the ion transporters change their expression profiles and hence are suggested to be a plausible target to improve crops for increased agricultural production (Schroeder et al. 2013). Plasma membrane ion transporters primarily extrude and transport long-distance Na+ and Cl−. Plasma membrane transporters are also critical for K+ acquisition during K+ starved conditions. On the contrary, intracellular ion transporters primarily involve the sequestration of Na+ and Cl− and control the cytoplasmic K+/Na+ ratio by releasing K+ into the cytoplasm. Despite the importance of the membrane proteins in plant salinity stress response, some aspects of the membrane proteins are remained unexplored, such as identifying the relevant membrane protein-lipid and membrane protein–protein interactions. Lipids are critical for membrane protein function. Salinity stress induces the restructuring of the plant cell plasma membrane due to the osmotic imbalance (Mansour et al. 2015). Production of ROS due to salinity stress also affects membrane lipid compositions and structure (Mansour et al. 2015). Lipids in the membrane control the regulation and activity of membrane protein. Therefore, it is evident that alteration of the lipid composition and structure in the membrane could regulate the membrane protein distribution, function, and activity. Although plenty of work has been done on protein-lipid interaction in animal and bacterial systems, such studies are very limited in plants due to several technical difficulties. Besides, membrane protein–protein interaction is evident in salinity stress response. Such protein–protein interaction in the membrane includes the communications between the receptor-like kinase and its immediate membrane protein substrate, membrane remodeling osmo- and ion-sensors and its subsequent transporters, channels providing ion gradient for transporter function, and finally, the H+-pump empowering the secondary active transporters. Identifying the critical protein–protein interaction in plants could also provide valuable information about the protein interaction network responsible for salinity stress response. The membrane protein interaction could be understood by correlating membrane proteomics and lipidomics data in differential salt treatment experiments. Another crude yet easy and direct alternative could be finding the interacting lipids and protein from the heterologous expression of plant membrane proteins (Dutta et al. 2020).

Recently, it has been suggested that adopting halophytic traits in crops could solve the salinity stress problem in agriculture (Liu et al. 2020). One significant difference between halophytes compared to salt-sensitive crops is the differential expression pattern of the membrane proteins (Assaha et al. 2017). Changes in protein expression patterns also suggest an altered protein–protein and protein-lipid interaction network in halophytes. Knowledge of such specific interactions may be essential because they can be targeted, and strategies could be developed to modulate their interactions. Additionally, membrane protein distribution in plant organs and its polarity in a cell could be changed by the distribution of the lipids. It is possible to target the specific membrane lipid synthetic pathway and their targeting to alter membrane protein distribution or polarity.