Role of the plasma membrane in saline conditions: lipids and proteins.
Salinity is a major environmental challenge affecting seriously plant growth and production. About 1000 million hectares, 7 % of the total land surface, is saline (Munns & Tester, 2008). The salinity problem is even worth in semiarid and arid regions where about one third of the world irrigated land suffering from secondary salinization (Munns & Tester, 2008). The injurious effects of salinity on plants are associated with ionic, osmotic and oxidative stresses (Mansour, 2013). Ionic component of salinity is related to toxicity of particular ionic species (e.g., [Na.sup.+] or [Cl.sup.-] stress) to plants as well as nutrient imbalance. High soil salt concentration reduces the soil water potential resulting in osmotic stress or water deficit. Salt stress also induces formation of singlet oxygen, superoxide anion, hydrogen peroxide and hydroxyl radical and hence causes oxidative stress in many plants (Sharma et al., 2012). Unfortunately, the majority of crop plants is relatively salt sensitive and is unable to tolerate low level of salinity. This necessitates an urgent need for research to develop tolerant crop plants to meet the demand for food all over the world. A close cooperation among scientists of several disciplines; plant physiology, molecular biology, and plant breeding is needed in order to achieve this goal. This strategy needs to characterize first the physiological traits that confer tolerance to high salinity and then molecular biologists and breeding programs can work to develop salt tolerant cultivars for crop plants. Understanding the role of the PM components, as an important cellular site for salt stress and tolerance, in adaptation to salinity will affirmatively participates in achieving this task.
The crucial role of the PM in acclimation to stresses is based on the fact that maintenance of the PM integrity under environmental threats has been reported to participate greatly in plant tolerance to different stresses (Zhang et al., 2010; Mansour, 2013; Jager et al., 2014; Maejima et al., 2014). Evidence supporting the implication of the PM integrity maintenance in adaptation to salinity as well as other stresses is addressed. Maintaining the PM stability has been demonstrated to be crucial for proper cell and plant performance under salt stress (Farooq & Azam, 2006; Ahn & Zimmerman, 2006; Ashraf & Ali, 2008; Collado et al., 2010; Mansour, 2013; Anbu & Sivasankaramoorthy, 2014). Presoaking of flax seeds in stigmasterol increased salt tolerance by improving membrane stability index and photosynthetic activity (Bassuany et al., 2014). In addition, the pivotal role of the PM stability maintenance in salinity tolerance is supported by the finding that NaCl-induced [K.sup.+] efflux is a result of the PM disintegrity and not due to ion channel mediation in rice (Coskun et al., 2013). Further support for the key role of PM composition in salt tolerance is the fact that PM lipids and proteins of tolerant plants are protected from oxidative attack, through enhancing antioxidant systems, a mechanism that minimizes lipid and protein oxidation and retaining the PM integrity (Alvarez-Pizarro et al., 2009; Collado et al., 2010; Gill & Tuteja, 2010; Mansour, 2013). Moreover, damage to the PM has been found to be associated with changes in membrane physical structure and/ or chemical properties, and thus increased salt sensitivity in response to salinity (Huang, 2006a). Agents that accumulate and improve salt tolerance have been also reported to protect and maintain the PM integrity under salt treatment (Mansour, 1995b, 1998, 2000; Mansour & Al-Mutawa, 1999; Mansour et al., 2002). Introduction of the carrot HSP17.7 (heat shock protein) into potato also maintained cell membrane stability, which enhanced tuberization (Ahn & Zimmerman, 2006). It is interesting to note that heat shock proteins are stress-responsive proteins produced under various stresses, and have been shown to protect the PM components (Wang et al., 2004). Cell membrane stability has been similarly indicated as a measure of salt tolerance in canola (Ashraf & Ali, 2008). Because of its critical roles in adaptation of plants to saline conditions, it is not hence unexpected that several studies believe that the PM might be a primary site of salt injury and salt tolerance (Leopold & Willing, 1984; Cramer et al., 1985; Lauchli, 1990; Mansour & Salama, 2004; Flowers & Flowers, 2005; Mansour, 1997, 2013, 2014). We therefore propose that the PM components must have or undergo certain compositional and structural alterations in order to maintain the PM stability and thus withstand high salt. These alterations are expected to be in a sustainable direction to maintain PM functionality and hence ion homeostasis in salt tolerant species under salinity. Salt sensitive species/cultivars, however, may lack such mechanisms under high salt stress. Figure 1 summarizes the salt stress signals that trigger gene expression changes, which resulting in stress-responsive mechanisms to reestablish homeostasis, protect and repair damaged PM and proteins. Figure 1 shows that improved salt tolerance can be attained by altering the PM proteins and lipids in saline environments.
Lipids and proteins are the staple ingredients of the PM. The PM is highly dynamic and different environmental stresses result in multiple changes in its organization. The key role of the PM is therefore based on the fact that the PM has a wide range of crucial functions in response to environmental stresses. These functions are essentially controlled by the PM lipids and proteins. The PM lipids are responsible for determining biological properties of the membrane (Uitert et al., 2010), and their composition was remarkably different and underlying variations in stress tolerance among crop species (Khan et al., 2009; Huynh et al., 2012; Mansour, 2013; Maejima et al., 2014; Scotti-Campos et al., 2014). It is therefore proposed the PM as a major target of environmental stresses, and changes in its lipid composition were related with increased resistance to different stresses (Mansour & Salama, 2004; Rodnguez-Vargas et al., 2007; Su et al., 2009; Huynh et al, 2012; Kosova et al., 2013; Mansour 2013, 2014; Scotti-Campos et al., 2014; Maejima et al., 2014). Evidence indicates that saline environments change the lipid composition/content of the PM, which proposed to contribute to salinity adaptation (Douglas, 1985; Mansour et al., 1994, 2002; Kerkeb et al., 2001; Wu et al., 2005; Bing-jun et al., 2005; Salama et al., 2007; Bargmann et al., 2009; Zamani et al., 2010). It is also suggested that specific PM lipid species may correlate with salt tolerance (Kerkeb et al., 2001; Mansour et al., 2003; Mansour & Salama, 2004; Rodriguez-Vargas et al., 2007). High salinity results also in changing the PM transport systems, PM general proteins as well as its fluidity and permeability (Mansour et al., 2003; Salama et al., 2007; Ghaffari et al., 2014; Mansour, 2013, 2014), which have great impact on plant differential responses to salinity. The prominent role of the PM lipid composition in regulating the activity of PM-associated transport systems is documented (Carruthers & Melchoir, 1986; Cooke & Burden, 1990; Cooke et al., 1993, 1994), which greatly affects ion homeostasis and in turn tolerance to high salinity (Mansour, 2014). Further evidence supporting the involvement of the PM lipids in salt tolerance is that expression of genes coding for major membrane lipid biosynthetic enzymes and fatty acid desaturases demonstrate a possible relationship between the variations in membrane lipid composition and tolerance to stresses (Allakhverdiev et al., 1999; Huynh et al., 2012; Zhai et al., 2012). Moreover, the PM components have a pivotal role in cellular signal transduction under different stresses (Wang et al., 2008a; Lu et al., 2012; Klinkenberg et al., 2014; Ruelland et al., 2014). Salinity stress, like other stresses, is perceived at the PM, which then triggers intracellular-signaling cascades that modulate gene expression, and consequently responses leading to salt stress tolerance (Fig. 1). It is therefore anticipated that salt tolerant cultivars of various plant species may maintain the PM lipids in terms of quantity and quality, whereas sensitive ones lack such mechanism of adjustment.
Proteomics of the PM has been demonstrated as one of the most important adaptation mechanisms to environmental stresses (Hong & Hwang, 2009; Zamani et al., 2010; Takahashi et al., 2013). In support to that, Takahashi et al. (2013) reported adaptations of the PM functions to low temperature to be associated with alterations of its protein composition during acclimation. Further evidence is that the pepper CaPIMP1 gene encodes a PM protein involving in plant stress tolerance in adverse environmental conditions (Hong & Hwang, 2009). Many investigations report qualitative and quantitative differences in the PM proteins of plant species/genotypes contrasting in salt sensitivity under saline conditions (Kononowicz et al., 1994; Kerkeb et al., 2001; Goncalo et al., 2003; Salama et al., 2007; Katz et al., 2007; Sengupta & Majumder, 2009; Zamani et al., 2010; Kosova et al., 2013; Mansour, 2013, 2014). These studies illustrate that several of salt responsive PM proteins improve plant salt tolerance under high salinity. The molecular bases of the observed differences include the fact that tolerant plants are able to maintain adaptive biosynthetic activities at high salinity (Lin & Wu, 1996; Babakov et al., 2000; Cheng et al., 2009; Mansour, 2013). Among salt responsive PM proteins, we mention protective proteins, transport proteins and sensory proteins, which has been shown that overexperssion of the genes encoding these proteins contribute to enhancing tolerance to high salinity (Osakabe et al., 2013; Mansour, 2014; Wang et al., 2014). From the above data, it appears that the capacity to maintain the proper functioning of lipid and protein biosynthetic activities and hence the stability and performance of the PM may help the plants to withstand the stress. The review thus focuses on the data drawn from the responses of the PM lipids and proteins to salt stress in plant species/cultivars contrasting in their response to salinity. These issues will be discussed in this contribution. The hypothesis that the PM lipid and protein composition/structure may be involved in plant adaptation to high salinity is also tested.
Response of the PM Components to Saline Conditions
The PM Lipids and Salt Tolerance
Lipids play vital roles in cellular structure and organization, signal transduction, trafficking, sorting of macromolecules, and are particularly essential in adaptation to extreme environments in microorganisms, plants and algae (Huang, 2006a; Lu et al., 2012). The critical role of the PM lipids in salt tolerance comes from the fact that membrane lipids have a great impact not only on changing the membrane integrity, permeability and fluidity but also on modulating transport proteins activity (Cooke & Burden, 1990; Venken et al., 1991; Mansour, 1995a; Yu et al., 1999; Mansour et al., 2003; Martz et al., 2006; Wassail & Stillwell, 2009; Lopez-Perez et al., 2009; Zamani et al., 2010; Mansour, 2013). The lipid requirements of transport systems have been addressed, and membrane lipid microenvironment is illustrated to be more effective than the membrane bulk lipids in this respect (Lee, 1991; Cooke & Burden, 1990; Cooke et al., 1993, 1994). Lipid microenvironment significantly influences the PM transport protein kinetic properties and efficiency under salinity (Palmgren & Sommarin, 1989; Mansour et al., 2003; Amtmann & Beilby, 2010; Gutla et al., 2012; Mansour, 2014). In addition, the impact of the PM lipids on its integrity and functions are brought about by lipid influence on the physical and structural properties of the PM (Shinitzky, 1984; Russell, 1989). Further evidence supporting the PM lipid contribution to salt tolerance comes from the finding that overexpression of enzymes that affect one membrane lipid component modulate tolerance to different environmental challenges (Kim et al., 2005; Ryan et al., 2007). Furthermore, overexpression of OsSPLl (sphingosine-1-phosphate lyase gene) in transgenic tobacco reduces salt stress tolerance, indicating that this gene may be responsible for the reduced tolerance in transgenic tobacco plants under salt stress (Zhang et al., 2012a). Sphingolipids, including sphingosine-1-phosphate, have been shown to function as signaling mediators to regulate diverse aspects of plant growth, development, and stress response (Zhang et al., 2012a).
It is demonstrated that changes in PM lipids correlate with salt tolerance through lipids effect on the PM [H.sup.+]-ATPase activity in saline environment (Lin & Wu, 1996; Mansour et al., 2003; Alvarez-Pizarro et al., 2009). In accordance, lipid requirements of the PM ATPases from oat roots are shown (Serrano et al., 1988). Differences in the PM ATPase activities were thus a consequence of differences in the PM lipid composition of oat root and coleoptile (Kasamo & Nouchi, 1987; Sandstrom & Cleland, 1989a). The authors also demonstrated the phospholipid requirement for activation of proton translocating activity by PM ATPase. In support to a specific requirement of lipid environment for the PM ATPase optimal activity is the fact that salt tolerant barley cultivar treated with linoleic acid (18:2) increased the root PM [H.sup.+]-ATPase activity (Yu et al, 1999). This effect was consistent with the lower [Na.sup.+] content and [Na.sup.+]/[K.sup.+] ratio in leaves of the tolerant cultivar under salt stress. This is because the PM [H.sup.+]-ATPase is known to energize the PM for [Na.sup.+] exclusion by [Na.sup.+]/[H.sup.+] antiporter. Moreover, the PM [H.sup.+]-ATPase activity increases in vitro after the addition of linoleic acid as well as other fatty acids (Palmgren et al., 1988). Different sterol species have been also found to modulate the PM [H.sup.+]-ATPase activity differently and also had unique effect on different plant species (Cooke et al., 1993; Grandmougin-Ferjani et al., 1997). Sandstrom and Cleland (1989b) similarly demonstrated the essentiality of sterol species for the oat root PM [H.sup.+]-ATPase activation. Furthermore, modifications of the broccoli root PM lipid composition affect the activity of the PM aquaporins, which was reported to provide a mechanism for controlling water permeability under salinity stress (Lopez-Perez et al., 2009). Alteration in the PM lipids also affects [Na.sup.+]/[H.sup.+] antiporter, as genetic engineering of unsaturation of membrane fatty acids increases Synechocystis [Na.sup.+]/[H.sup.+] antiporter activity (Allakhverdiev et al., 1999). In the same trend, polyunsaturated fatty acids have been reported to modulate ion channels activities (Gutla et al., 2012). It is obvious that alterations in the PM lipid composition under high salinity may have advantage for modulating the transport systems and hence ion homeostasis, and consequently the plant cells can cope with the injurious impact of the salt stress. Darwish et al. (2009) demonstrate, however, that salt stress induces several lipid responses in rice leaves but these responses do not explain the difference in salt tolerance between sensitive and tolerant cultivars. It is most likely that studies on tissue level may mask possible great differences at the membrane molecular level between cultivars contrasting in salt tolerance, as far as a specific PM lipid species is concerned. It is rather crucial to investigate the lipid responses to salinity at specific membrane molecular level.
Production of biologically active lipid molecules (e.g., phosphatidic acid, PA) has been shown to play an important role in salt stress response and tolerance (Ruelland et al., 2014). It is known that PA results from the action of phospholipases and/or lipid kinases. Many studies imply PA as a key signaling molecule in plant responses to saline conditions (Yu et al., 2010; Ruelland et al., 2014). The importance of PA production in response to salinity is supported by the fact that PLD[alpha]1-deficeient mutants of Arabidopsis showed drastic decrease in salt tolerance (Yu et al., 2010). Further evidence is provided from the study of Shen et al. (2011) on rice suspension-cultured, in which rice phospholipase D[alpha] mediated [H.sup.+]-ATPase activity and transcription and hence is involved in salt tolerance. It has been therefore reported that plants overexpressing phospholipase genes frequently display tolerance to high salinity (Ruelland et al., 2014). In addition, [PLA.sub.2] is also implicated in salt stress responses, as it has been demonstrated to mediate a defensive ROS production in salt-stressed wheat. Lipid signaling pathways have been also illustrated to be involved in the regulation of the level of proline under salt stress (Ruelland et al., 2014). Proline is believed to play an adaptive role and contributes to salt tolerance in several crop species (Mansour, 1998, 2000). Lipid signaling implication in plant stress responses can be summarized as follows: information transmission between the PM, cytosol and other organelles occurs as PM perceives (i.e., PM lipid and protein molecules) the salt signal, and offer a medium for the action of lipid processing inducible enzymes. The lipid and protein mediators (e.g., PA, protein kinases), involved in plant responses to stress, are then produced. The majority of lipid mediators stay transiently in the PM. Binding of the lipid mediators with soluble proteins (e.g., MAPKs, CDPKs), however, allows the transduction of the signal into the cell. These proteins affect the expression of major stress responsive genes leading to physiological responses (Fig. 2). In addition, the stress, as the primary signal, induces hormone synthesis (e.g., ABA, salicylic acid and jasmonic acid), which act as a secondary signal and also they have been found to stimulate plant adaptive responses. It is interesting to mention that Bing et al. (2013) reported that overexpression of atSTK, a serine-threonine protein kinase of Arabidopsis, improved Arabidopsis salt tolerance. The increased salt tolerance was owing to reduced PM permeability, increased proline content and decreased lipid peroxidation. The study also indicated that atSTK transfer the salt stress signal in Arabidopsis through the MAPK pathway. Further evidence supporting the PM lipids implication in the perception and transmission of salt external information and hence playing a major part in salt adaption is the report that phospholipid cleaving enzymes, phosphoinositol 4,5-bisphosphate, diacylglycerol, unsaturated fatty acids and phosphatidic acid serve as key signaling molecules (Golldack et al., 2014, Klinkenberg et al., 2014), and therefore play a prime role in responses of plants to environmental stresses and tolerance. Phospholipid signaling pathways and formation of PA as a key signaling molecules in plant responses to salt stress is summarized in Fig. 3. As illustrated in the Fig. 3, the action of phospholipases and/or lipid kinases results in production of biologically active lipids for salt stress signaling and transduction. In the following sections, the response and role of the PM lipid species (i.e., phospholipids, glycolipids, sterols, fatty acids) in adaptation to salt imposition are discussed.
The PM Total Lipids
As the preservation of the PM integrity depends on its lipid composition, published reports therefore indicate that total lipid composition of the PM is important for salt resistance of plants (Russell et al., 1995; Lin & Wu, 1996; Huang, 2006a; Upchurch, 2008; Lopez-Perez et al., 2009; Zamani et al., 2010; Lu et al., 2012; Mansour, 2013). Preservation of the PM integrity under saline conditions may result from maintained or increased lipid level of the PM. Alteration in the PM total lipids suggests a stimulation of membrane biosynthesis in order to accommodate the PM stability and signal transduction under NaCl stress. Moreover, the PM lipid increase may have a positive point as causing an elevation of the total membrane area of the cells under saline conditions. This new status of the PM may help tolerant plants to maintain the essential activity of membrane intrinsic proteins for exclusion of toxic ions from the cells (Kuiper, 1985; Blits & Gallagher, 1990). On the other hand, impaired PM total lipids in salt sensitive plants may result from the salt-induced lipid peroxidation and degradation. Salinity-induced decrease in the PM lipid content may also be interpreted as caused by a reduction in lipid biosynthesis via reducing expression of lipid biosynthetic enzymes. Evidence indicates that under saline conditions salt tolerant cultivars of various plant species maintain PM lipids in terms of quantity and quality, whereas sensitive ones lack such mechanism of adjustment (Kuiper, 1984; Mazliak, 1989; Lin & Wu, 1996; Lu et al., 2012; Mansour, 1997, 2013). Total PM lipids from roots and leaves increase under salinity was correlated with soybean cultivars salt tolerance (Bing-jun et al., 2005). In addition, total lipid content of the shoot of the halophyte Suaeda altissima treated with 250 mM NaCl was more than 2.5-fold higher than that when plants were grown under 1 mM NaCl (Tsydendambaev et al., 2013). Salt treatment resulted also in increased the PM total lipid of salt adapted cells of the cyanobacterium Anacystis nidulans (Molitor et al., 1990). In accordance, maintenance of the PM lipid composition in Dinaliella salina under high salinity has been reported as an adaptive mechanism to cope with the external salt (Peeler et al., 1989). NaCl treatment also increased the PM total lipids in the snow alga Chlamydomonas nivalis (Lu et al., 2012). Moreover, exposure of Catharanthus roseus cell suspensions to salt stress enhanced membrane total lipid content (Elkahoui et al., 2004). Guimaraes et al. (2011) report that membrane total lipids decreased in leaves of cowpea under salt treatment was associated with increased lipid peroxidation, membrane damage and salt sensitivity. The lipid contents in both roots and shoots decreased dramatically in the salt sensitive rice (Huynh et al., 2012) and sensitive maize Chaffai et al. (2005) cultivars. In the tolerant cultivars, however, the contents of the major root and shoot lipid classes remained remarkably stable. The authors suggested that decreases in membrane lipids in the sensitive cultivars may have negative consequences on the physiology of the plant, such as a decrease in mineral absorption. Furthermore, major PM lipid classes remained stable in calli of a salt marsh grass, Spartina patens, in response to salinity, which was associated with stable membrane fluidity (Wu et al., 2005). In the same trend, root membrane total lipids remain relatively unchanged in halophytic barley whilst it is decreased in Hordeum vulgare in response to NaCl treatment (Chalbi et al., 2013). In roots of the halotolerant species Cochlearia anglica lipid content increased considerably under exposure to NaCl, and also the relative proportions of phospholipids, galactolipids and neutral lipids or the fatty acids remained unchanged (Prud'homme et al., 1990). NaCl treatment similarly decreased total lipid content of the PM from roots of salt sensitive wheat cultivar (Mansour et al., 1994). Further evidence is that barley root PM lipid composition was not affected under salt stress, which was interpreted as maintenance of a constant insensitive PM lipid composition to salt (Brown & DuPont, 1989). From the above results, it can be concluded that maintenance of the PM lipid composition is important for plant survival under salinity. It is also inferred that the PM total lipid quantity and quality is more stable in salt tolerant plants, which may contribute to higher PM stability and salt tolerance in saline conditions.
Besides alterations in lipid biosynthetic activities induced by salinity, the molecular bases of the observed differences in the PM lipid content also include the fact that PM lipids of tolerant plants are protected from peroxidative attack (Sharma et al., 2012). This occurs through enhancing antioxidant systems in salt tolerant plants, a mechanism that minimizes lipid peroxidation and favor maintenance of the PM lipids and integrity (Alvarez-Pizarro et al., 2009; Collado et al., 2010; Gill & Tuteja, 2010; Mansour, 2013). It has been also reported that cellular injury induced by salinity is linked to increased lipid peroxidation (Huang, 2006a), as the fatty acid double bonds are the site for reactive oxygen species attack and hence lipid peroxidation. In support to that, Crkl-1 (CRKs are a type of serine-threonine protein kinase) transformants had a decreased tolerance to salt stress compared with wild Arabidopsis (Tao & Lu, 2013). The decreased salt tolerance was related to higher membrane lipid peroxidation in crkl1-1 plants, indicative of an important role of membrane lipid preservation in salt tolerance. Moreover, lipid peroxidation was greater in root of salt sensitive wheat and cotton cultivars relative to salt tolerant ones under saline conditions (Ghogdi et al., 2013; Kumari et al., 2013). The PM-enriched vesicles from salt tolerant dwarf cashew roots similarly had unchanged level of peroxidated lipid while lipid peroxidation was remarkably increased in salt sensitive one (Alvarez-Pizarro et al., 2009). The study also indicates that improved protection of salt tolerant roots may have resulted from higher accumulation of proline in this organ. This conclusion agrees with the fact that proline has been shown to protect the PM of onion inner epidermal cells against salt stress (Mansour, 1998, 2000). In other plant species, the level of lipid peroxidation has been used as a marker of tolerance to salt-induced oxidative stress (Yang et al., 2004; Demiral & Turkan, 2005). Stark (2005) also reports that enhanced lipid peroxidation may lead to functional alterations of the PM and thus increases susceptibility to salt. Taken together, it is obvious that the PM lipid protection from salt-induced oxidative stress is vital in saline conditions. It is also reasonable to infer that the PM lipid composition is different in salt contrasting cultivars, which contributes to salt adaptation.
The PM Phospholipids
Phospholipids are one class of the membrane lipids, and they constitute a major component of the membrane as they can form lipid bilayers. The PM phospholipid species and abundance from different species/cultivars contrasting in salt tolerance are changed in response to saline conditions (Mansour et al., 1994, 2002; Kerkeb et al., 2001; Wu et al., 2005; Salama et al., 2007; Zamani et al., 2010), suggestive of their role in salt acclimation. Evidence is provided that the changes in the PM phospholipids have been proposed to be correlated with adaptation to saline environments (Kuiper, 1984; Mansour & Salama, 2004; Alvarez-Pizarro et al., 2009; Lu et al., 2012; Mansour, 2013). The PM phospholipid changes are most likely promote maintenance of the membrane integrity and cellular homeostasis in salt tolerant species/cultivars in saline environments. It is important to mention that molecular percentage of the PM phospholipids was already different in the root PM of non-salinized salt tolerant and sensitive maize cultivars, which further varied differently in response to salinity (Salama et al., 2007), further supporting for the PM phospholipid involvement in salt tolerance. The root PM total phospholipids decreased in salt sensitive wheat and maize cultivars, whereas it did not change in salt tolerant ones in response to salt treatment (Mansour et al., 1994; Salama et al., 2007). In agreement with that, the PM phospholipid contents of the roots and leaves increased in salt tolerant soybean cultivar whereas it decreased in sensitive cultivars, which was suggested to reduce PM permeability to injurious ions in tolerant cultivar under saline conditions (Bing-Jun et al., 2005). In addition, Kerkeb et al. (2001) found that the PM isolated from tomato calli tolerant to 100 mM NaCl exhibited higher phospholipids content relative to sensitive one. Liang et al. (2006) also reported absence of significant changes in total phospholipid content in root PM from salt tolerant barley genotype. On contrary, total phospholipids content was greater in salt sensitive dwarf cashew root PM than in tolerant one after salt treatment (Alvarez-Pizarro et al., 2009). It is unclear whether this reduction in the root PM total phospholipids of a salt tolerant cultivar has any adaptive significance in response to salt stress. It seems, however, that maintenance or increasing the PM phospholipid contents may have an adaptive value for ultrastructural alterations of the PM under salinity. These alterations most probably participate in retaining the PM integrity in saline environments. Such PM adaptation may be, however, lacking in salt sensitive plants.
Different lipid species within the same lipid class play different roles in the regulation mechanism on stress response and tolerance (Kuiper, 1984; Russell, 1989; Wassail & Stillwell, 2009). Some membrane phospholipids tend to form bilayer or lamellar structure (e.g., phosphatidylcholine, PC; phosphatidylglycerol, PG), whereas others are inverted hexagonal phase or nonbilayer forming lipids (e.g., phosphatidylethanolamine, PE), which has a great impact on the PM functions and properties (Quinn, 1983; Gagne et al., 1985; Russell, 1989; Lu et al., 2012; Mansour, 2013). Nonlamellar domain in the membrane also causes interruption of the bilayer structure and hence renders high permeability (Russell, 1989), which influences ion absorption under salinity. The decrease in PC to PE ratio in wheat root PM under salinity (Mansour et al., 1994) and in oat root in response to dehydration (Norberg and Liljenberg, 1991) was suggested to disrupt the PM integrity of these sensitive cultivars. Similarly, salt stress decreased membrane PC in roots of sensitive tomato cultivar (Racagni et al., 2003). NaCl stress, However, unchanged this ratio in the halophyte Spartina patens callus (Wu et al., 2005), suggestive of a possible role of greater bilayer forming lipids (PC) in salt tolerance (Table 1). Membrane PC also was increased in the root of salt tolerant Plantago species after salt treatment (Kuiper, 1984). It is also worth noting that exogenously applied choline, which metabolized into PC, stimulated wheat salt tolerance (Mansour et al., 1993), supportive of the possible role of PC in response to salt stress. Further evidence for the importance of specific change in individual molecular species of the PM lipids in adaptation to environmental stresses is provided by the finding that phospholipids, particularly PC, decreased dramatically in root and shoot of [Al.sup.3+] sensitive rice cultivars compared with tolerant ones (Huynh et al., 2012). The authors suggest that the capacity to maintain the proper functioning of some lipid biosynthetic activities and hence the stability of lipid composition may help the rice plant to withstand [Al.sup.3+] stress. Furthermore, Zhang et al. (1997) found also an increase in PC from root PM of [Al.sup.3+] tolerant wheat cultivar under [Al.sup.3+] treatment. Increasing evidence suggests therefore a major role for PC in plant stress adaptation (Kuiper, 1984; Tasseva et al., 2004; Mansour, 2013). A role for the PM PC in adaptation to salt stress is hence suggested (Table 1). In addition, the root PM PG of salt tolerant canola cultivars was increased and PC decreased under salinity (Zamani et al., 2010). Similarly, the PM PG increased whereas PE decreased in maize tolerant cultivar, which was interpreted as alterations that maintain the PM integrity and functions in saline conditions (Salama et al., 2007). Salt-induced PM phospholipid changes (more reduction in PG/PE ratio and increased in PI level) was correlated with [Cl.sup.-] accumulation in salt sensitive maize cultivar (Salama et al., 2007). A decrease in PE of the PM and an increase in PG have been also reported in salt tolerant buffalo grass clone (Lin & Wu, 1996) and halophilic cyanobacteria Aphanothece halophytica (Ritter & Yopp, 1993). It is important to note that in the previous works the impact of decreased PC on the PM integrity of salt tolerant cutlivars is most likely compensated for by the increased PG which also tends to form bilayer configuration. The data in Table 1 suggests a possible relationship between increasing the PM PG and salt tolerance. Another PM phospholipid species that might play a role in salt tolerance is phosphatidylinositol (PI): it increased significantly in roots of salt sensitive maize (Salama et al., 2007), sensitive canola (Zamani et al., 2010; Bybordi, 2011), sensitive wheat (Mansour et al., 1994) and sensitive tomato (Racagni et al, 2003) relative to tolerant ones, indicative of a possible role in salt adaptation. Evidence is provided, however, that changes in PI phosphorylation in plants are associated with salt stress and tolerance (Ruelland et al., 2014), despite PI was decreased in salt tolerant plants in the previous publications. PI has been proposed to play a role as signaling molecule in response to stresses (Golldack et al., 2014). It appears therefore that formation of other biologically active lipid molecules (e.g., PA) are rather come into play as key signaling molecules when PI was deceased in salt tolerant cultivars. Based on the aforementioned data, we suggest increased PM abundance of PI to be correlated with salt sensitivity, whereas elevated PC or PG may be associated with salt adaptation (Table 1). Accordingly, it is inferred that individual molecular species of a particular PM lipids might play a role in plant adaptation to salt stress.
Changes in specific ratios of the PM lipid classes could also be crucial for salt tolerance. A higher PM free sterols/phospholipids ratio was demonstrated in salt tolerant tomato calli relative to sensitive calli (Kerkeb et al., 2001). Mansour (2013) cited in his review several publications report a higher sterols/phospholipids ratio in the root PM of different salt tolerant cultivars exposed to salinity. Furthermore, Zamani et al. (2010) illustrated increased PM sterol/phospholipids ratio in tolerant canola cultivars in response to salinity. High salt similarly increased the PM sterols/ phospholipids ratio of wheat roots (Mansour et al., 2002) and of salt tolerant citrus roots (Douglas & Walker, 1984). A stable free sterol/phospholipid ratio was also demonstrated in the PM of halophyte Spartina patens callus (Wu et al., 2005), of wheat roots (Mansour et al., 1994), of Dnnaliella salina (Peeler et al., 1989) and of barley roots (Brown & DuPont, 1989) in response to salinity. In addition, the PM sterols/phospholipids ratio was increased in the root of salt tolerant maize cultivar, but decreased in sensitive one under high salinity (Salama et al., 2007). In accordance with these results, an increase in this ratio of the PM was correlated with salt tolerance in canola cultivars (Bybordi, 2011). Similarly, lower proportion of phospholipids in the rice root tips bring about lower surface negativity of the PM, leading to less permeability and less binding of [Al.sup.3+], and hence induced tolerance to [Al.sup.3+] (Huynh et al., 2012). The PM phospholipid/sterol ratio is also lower in [Al.sup.3+] tolerant rice cultivars than sensitive cultivars (Khan et al., 2009), and modification of this ratio by sterol synthesis inhibitors reduced [Al.sup.3+] tolerance of rice tolerant cultivar. NaCl stress also increases the PM sterols/phospholipids ratio of marine yeast Debaryomyces hansenii (Turk et al., 2007). The molecular significance of the higher sterols/phospholipids ratio in acclimation to salinity is its contribution to membrane rigidity and thus reduced NaCl permeability (Wu et al., 1998). In addition to the above results, further evidence was provided that a less fluid bilayer was regarded as an adaptive feature for reduced passive NaCl influx to cytosol (Kuiper, 1984; Mansour et al., 1994; Mansour, 2013). It is therefore conceivable to suggest that maintaining or increased the PM sterol/phospholipid ratio may play role in salt tolerance. This contention has been also proposed by Kuiper (1984), Mansour (2013) and Mansour and Salama (2004). It is important to mention that the role of decreased membrane fluidity in toxic ion absorption reduction and hence salt tolerance may apparently disagree with the relationship between increased membrane fluidity and salt tolerance discussed below. In general, one of decisive roles of the PM in plant tolerance to saline environments rely on the fact that impainnent of membrane integrity and in turn its fluidity has a great impact on acclimation to high salinity. Moreover, the influence of fatty acid unsaturation on increasing the PM fluidity may override other impacts on the fluidity since an increase in sterol content may not always condense membranes (Chong et al., 2009). Besides the PM sterols/ phospholipids ratio, the glycolipids/phospholipids ratio may be also involved in plant salt tolerance under salinity. The PM glycolipids/phospholipids ratio was increased in roots of salt tolerant maize cultivar (Salama et al., 2007) and salt tolerant canola cultivars in response to salt treatment (Zamani et al., 2010; Bybordi, 2011). Furthermore, an increase in this ratio of the PM was related to haloadaptation of cowpea (Vazquez-Duhalt et al., 1991). The authors proposed that the greater this ratio is, the lower the membrane ion permeability and hence tolerance to salinity. On the other hand, the PM glycolipids/phospholipids ratio was increased in salt sensitive wheat cultivar (Mansour et al., 1994) and salt sensitive soybean cultivar (Bing-jun et al., 2005) under salt stress. Increased this ratio was proposed to enhance [Cl.sup.-] absorption in grape roots in saline condition (Bing-jun et al., 2005). Based on this apparent discrepancy, the role of the PM glycolipids/phospholipids ratio in salt tolerance is not yet clear and need further elucidation.
The PM Sterols
Sterols are important structural components of cell membranes ubiquitously present in all eukaryotic organisms, regulating membrane fluidity and permeability. The PM sterols implication on modulating the PM functions and properties, and thus plant performance is supported by the fact that sterols packing in the membrane bilayer would reduce its permeability (Van Blitterswijk et al., 1981; Shinitzky, 1984; Huang, 2006a). This effect would modulate ion uptake and transport in saline environments. Kerkeb et al. (2001) indicated that the PM isolated from tomato calli tolerant to high NaCl had higher sterols content compared with sensitive calli. The amount of total free sterols was also increased in diatom Nitzschia leavis with the increase in salt concentration (cf. Kumari et al., 2013), which was related to salt tolerance. In addition, studies on halophytic species point to the functional importance of high sterol content in lipid bilayer to cope with saline stress (Blits & Gallagher, 1990; Wu et al., 1998). In citrus rootstocks, Douglas and Walker (1984) showed that the salt exclusion capacity correlated well with the increase of the PM free sterol level in salt tolerant variety. Furthermore, salt tolerant barley genotype showed absence of variation in total free sterols content of root PM, suggesting that maintenance of the PM sterol is essential for its function under salinity (Kuiper, 1985; Liang et al., 2006). Total PM sterols also increased in root of tolerant canola cultivars under salinity (Zamani et al., 2010). Increasing the PM sterols under salinity raises the question of PM structural configuration as the greater the sterols in the PM is, the more packing of the bilayer (Douglas, 1985) and thus reducing ion permeability. In this connection, it has been demonstrated that changes in membrane lipids and packing greatly affect the activities of the membrane proteins (Lundbaeck et al., 2010). On contrast, there was an increase in the leaves of the PM total free sterols in barley genotype sensitive to salt, but this increase did not contribute to either the stimulation of the PM [H.sup.+]-ATPase or regulation of toxic ions movements through root PM (Liang et al., 2006). These results can be interpreted by the finding of Chong et al. (2009) who report that an increase in sterol content does not always condense membranes or make them more ordered. Total free sterols content was also greater in salt sensitive dwarf cashew root PM than in tolerant one after salt treatment (Alvarez-Pizarro et al., 2009). It appears that the increase in the PM sterols in sensitive genotype could be a salt deleterious effect since changes in the PM lipids under salinity are rather complicated. For instant, plants to maintain the PM integrity and functions in saline environments, one lipid change might be counterbalanced by others or may work together with others, and ultimately these alterations are anticipated to be in a favorable direction to maintain the PM stability and functionality in salt tolerant plants, but not so in sensitive ones. In light of the above, it seems that salt-induced increase in the PM total sterols of salt tolerant plants may be a prerequisite for the proper functioning of the PM and thus may have an adaptive significance. On contrast, the increase in the PM sterols of salt sensitive plants may be overcome by unfavorable other lipid alterations, and hence have no advantages for plant performance under stress conditions.
Besides the PM total free sterol content, sterol composition appears to be crucial for salt tolerance. The PM sterols composition have been altered in different plant species under saline conditions, which was suggested as an adaptation mechanism to salinity (Mansour et al., 1994; Lin & Wu, 1996; Kerkeb et al., 2001; Wu et al., 2005; Salama et al., 2007; Bargmann et al., 2009, Lopez-Perez et al., 2009; Zamani et al., 2010; Bybordi, 2011). Compositional changes in free sterols species were reported under salinity: increase in campesterol and a decrease in sitosterol of PM of Spartina patens callus (Wu et al., 2005). The PM campesterol also increased in NaCl-tolerant tomato calli when treated with 100 MM NaCl (Kerkeb et al., 2001). In accordance, stigmasterol and minor planar sterol, cholesterol, of the wheat PM were increased under salinity (Mansour et al., 1994). It is reported that more planar sterols (campesterol, stigmasterol) have tighter packing in the phospholipid bilayer, and reduce PM permeability to ions and hence improve plant survival under salinity (Douglas, 1985). This in turn most likely enhances ion exclusion in saline conditions. In citrus cultivars, the root PM stigmasterol was increased whereas campesterol and sitosterol were decreased as the external NaCl was increased (Douglas, 1985). In salt tolerant citrus cultivar, increased more planar stigmasterol may play a role in ion exclusion under salinity, as it is proposed that membrane with high level of campesterol or stigmasterol would be less permeable to ions (Huang, 2006). Likewise, a decrease in the membrane campesterol or stigmasterol level would be detrimental under high salinity. In addition, planar sterol species are more effective in regulating membrane properties and integrity than less planar species, sitosterol (Mansour, 1997, 2013; Lopez-Perez et al., 2009). More planar sterol species have been therefore suggested to be correlated with salt tolerance in various crop species (Table 1, Kuiper, 1984; Mansour et al., 1994; Mansour & Salama, 2004; Lopez-Perez et al., 2009). Furthermore, the stigmasterol was increased while sitosterol was decreased in the PM of broccoli roots in response to salt treatment, which was interpreted as an adaptive mechanism to adjust both water and ion transport during the acclimation of the plants to saline environment (Lopez-Perez et al., 2009). The free sterols of Dunaliella salina changed only slightly when grown in high salinity (Peeler et al., 1989). Similarly, small changes in the relative abundance of the PM various sterols from barley roots grown in 100 mM NaCl (Brown & DuPont, 1989). The study demonstrated that salt-treated barley had a higher stigmasterol and lower sitosterol, with no change in cholesterol level. Further evidence for the importance of the planar sterol in adaptation of plants to salt stress is provided by the fact that stigmasterol priming enhanced salt tolerance of flax plants (Bassuany et al., 2014). The results imply that retaining or increasing more planar sterols in salt tolerant plants may contribute to the PM integrity maintenance and thus salt tolerance. We suggest also that reducing less planar and increasing more planar sterols in the PM might be advantageous in ion exclusion and hence adaptation to saline conditions (Table 1).
Another line of evidence for the involvement of the PM sterols in salt tolerance comes from their key role in the regulation of transport systems, which have a great impact on ion homeostasis under salinity. The sterol modulation of the com root PM [H.sup.+]-ATPase activity was shown to be dependent on both the sterol concentration and the sterol species (Grandmougin-Ferjani et al., 1997). In addition, the efficiency of different sterols to control passive membrane permeability also varies greatly among sterol species. Cholesterol and stigmasterol were found to stimulate the PM proton pump from com roots, while sitosterol inhibits its activity. Cholesterol stimulates the PM ATPase at low and high concentrations whereas stigmasterol has stimulating effect at low concentration and inhibitory effect at high concentration (Grandmougin-Feijani et al., 1997). The results clearly highlight the differential effect of sterol class and concentration on affecting ATPase activity, which should be taken in consideration when interpreting the PM lipid alterations and tolerance to salinity. The results of Blits and Gallagher (1990) and Kerkeb et al. (2001) are further supporting the notion that ion exclusion capacity in tolerant cultivars is correlated with the changes in the level and composition of free sterols. Increased more planar sterols reduced the PM [H.sup.+]-ATPase activity in salt tolerant tomato calli in response to salt stress, which was reported to be correlated with salinity-induced a reduction in the PM fluidity (Kerkeb et al., 2001). Reduced PM fluidity is expected to be associated with decreased [Na.sup.+] and [Cl.sup.-] contents, but their observations indicate increased level of these ions. It seems that salt-induced reduction in proton pump activity of tolerant calli resulted in no PM energization required for [Na.sup.+] extmsion by [Na.sup.+]/[H.sup.+] antiporter activity, and therefore leads to [Na.sup.+] accumulation which might be sequestered in the vacuole of the salt tolerant calli. The results point out also to the possibility that reduced proton pump activity dominated the impact of decreased PM fluidity regarding the uptake of ions, which clearly accounts for the complex nature of the alterations occurring in the PM lipids under saline environment. The results imply, however, clear evidence for the importance of molecular sterol species in affecting the PM transport system activity, which may play a fundamental role in the ion exclusion mechanism and tolerance in high salinity.
The PM Fatty Acids
Fatty acids are major components of the membrane that regulate its fluidity as well as associated transport systems and enzymes. One crucial impact of the membrane fatty acids on membrane are their degree of saturation/unsaturation. Saturation/unsaturation degree is a decisive factor modulating membrane integrity, functions and properties. Unsaturated fatty acids play an essential role in the biophysical characteristics of the membrane and determine the proper function of its attached proteins. On the other hand, saturated fatty acids packing in the membrane bilayer would reduce its permeability and fluidity, because they are major components contributing to membrane rigidity (Van Blitterswijk et al., 1981; Shinitzky, 1984). The ability of cells to alter the degree of unsaturation/saturation in their membranes is thus anticipated to be an important factor in cellular acclimatization to environmental conditions. In response to saline environments, the PM fatty acids are altered differently in plant species/cultivars contrasting in their salt tolerance. When two maize cultivars contrasting in salt tolerance were grown in 100 mM NaCl, there was an increase in saturated fatty acids and in turn a decrease in unsaturated/saturated fatty acid ratio of the root PM, more so in salt tolerant cultivar (Salama et al., 2007). In this study, the molecular percentage of the PM fatty acids was already different in salt sensitive and tolerant cultivars in absence of the salt treatment, suggestive of the critical role of the PM fatty acids in varietal differences even without saline conditions. The PM saturated and unsaturated fatty acid composition and abundance were also contrasting in salt tolerant and sensitive canola cultivars in absence of salt treatment, and are further changed diversely under high salt (Zamani et al., 2010). In the work of Zamani et al. (2010), the root PM unsaturated/saturated fatty acid ratio was more decreased in salt tolerant canola cultivar than sensitive one in saline conditions. Increased salinity reduced the PM fluidity of halophyte Spartina patens calli, which was related with increased fatty acid saturation (Wu et al., 2005). Moreover, the degree of the PM fatty acid saturation was increased with increasing external salinity in halotolerant alga Dunaliella salina, which has been hypothesized to make the membrane less permeable to NaCl (Peeler et al., 1989). In the previous study the relative stability of the PM composition under salt stress was proposed as a successful adaptation to external NaCl. Adaptation of cyanobacterium Anacystis nidulans to high salinity was also associated with increased PM fatty acid saturation (Molitor et al., 1990), which has been reported to decrease membrane fluidity (Shinitzky, 1984). Molitor et al. (1990) also indicated that increased PM fatty acid saturation decreases permeability to added NaCl. Furthermore, greater reduction in unsaturated fatty acids has been reported to relate to a less fluid PM that reduces toxic ion permeability in various plants (Chaffai et al., 2005; Lu et al., 2012). Guimaraes et al. (2011) demonstrate that salinity stress increased membrane fatty acids saturation and saturated/unsaturated fatty acid ratio in cowpea leaves, leading to a reduction in cell membrane fluidity and increased salinity tolerance. Further evidence is provided that the PM fluidity and degree of unsaturation of fatty acids in the PM of salt tolerant yeast were decreased in the presence of 15 % NaCl in the culture medium (Hosono, 1992). The halophyte vegetative organs of Suaeda altissima treated with 250 mM NaCl had induced fatty acid saturation and elongation of their chain, which was considered as an adaptive response to reduce membrane permeability for ions under salt imposition (Tsydendambaev et al., 2013). Moreover, membrane polyunsaturated fatty acids as well as total fatty acids were decreased whereas saturated fatty acids were increased in borage leaves under high salinity, which was considered as an adaptation to salinity (Jaffel-Hamza et al., 2013). The authors indicate that the decrease in fatty acid unsaturation under salt was due to a reduction in the desaturase activity, which suggested as an adaptive feature to salinity. Based on the above discussion, it is reasonable to suggest a correlation between the PM fatty acid saturation and adaptation to high salinity.
Lu et al. (2012) report that the increase in saturation degree of the PM-associated fatty acids has two advantages for plants under salt imposition: as to reduce membrane permeability to NaCl and susceptibility to oxidative attack. In agreement with that, Moller et al. (2007) illustrate that salt tolerant plants may protect against the oxidative effects of salts through restructuring their membranes with less polyunsaturated fatty acids. Further support is the fact that lipid peroxidation greatly increases in salt sensitive plants under salinity (Hajlaoui et al., 2009; Jaffel-Hamza et al., 2013). Accumulation of 18:2 rather than 18:3 in the sensitive cultivar was related to more lipid peroxidation and an alteration in fatty acid desaturase activity in saline environment. Lipid peroxidation remains, however, minimal or unchanged in salt tolerant plants. As many reports show correlation between increased PM fatty acid unsaturation and acclimation to high salt (next section), it is not clear to this point whether the observed reduction in unsaturation level should be interpreted as a defense mechanism or rather as an undesirable process reflecting the salinity-induced damage. It may be considered as adaptation mechanism enabling plants to grow under saline conditions through decreasing the PM fluidity and hence reduces its permeability to ions. Another argument for recognizing the decreased unsaturation as a defense mechanism is the fact that polyunsaturated fatty acids are highly sensitive to peroxidation. Thus, a decrease in their content may reduce the intensity of oxidative reactions in the PM and protect them against severe damage. It appears also that the PM fatty acid saturation might be advantageous for plant acclimation to saline conditions until it reaches an optimal threshold of saturation, above which the fatty acid saturation would be injurious for the PM and disturbs its functioning. It is obvious however that more detailed investigations should be carried out in this area for a full understanding of the possible link between the PM saturated fatty acids and salt tolerance.
In support to fatty acids role in plant adaptation to salt stress, Lopez-Perez et al. (2009) observed that salinity increased unsaturated fatty acid content in broccoli root cells, resulting in less compact and more fluid PM. Maintaining a high degree of fatty acid unsaturation in the broccoli root PM was suggested to control membrane physic-chemical properties to cope with salt stress (Table 1, Lopez-Perez et al., 2009). Other studies report that salt sensitive plants subjected to salt stress commonly show decreased levels of C18:3 in their membranes and experienced a reduction in membrane fluidity (Upchurch, 2008; Hajlaoui et al., 2009). An increase in membrane unsaturated fatty acids of Suaeda salsa also enhance salt tolerance through protection of photo-system II under salt stress (Sui et al., 2010). It is also established that salt tolerance is related to 18:2/18:3 ratio. A decrease in the ratio of 18:2/18:3 reduced salt tolerance of different halophyte plants (Ivanova et al., 2006), which was related to lowered membrane fluidity. In addition, increased level of 18:3/18:2 and 20:5/20:0 ratios in roots of salt tolerant com cultivar contributes to the tolerance of this cultivar to salt stress (Hajlaoui et al., 2009). The previous authors report that a decrease in membrane stability was greater in sensitive cultivar than tolerant one. Maintained membrane stability of salt tolerant cultivar was associated with an increase in polyunsaturated fatty acids (18:3, 25:5), lower lipid peroxidation and lower saturated fatty acids in tolerant cultivar. Lower 18:3 was obtained in the membranes of salt sensitive clone buffalo grass in response to salinity (Lin & Wu, 1996). Further supporting evidence for the involvement of the PM unsaturated fatty acids in plant adaptation to salt stress is reported by Upchurch (2008) where sensitive plants commonly exhibited low 18:3 in their membranes under salinity, suggesting declined level of 18:3 may be related to salt sensitivity (Table 1). From this data, it is conceivable to propose that a particular individual fatty acid molecular species may greatly affect the plant adaptation to salinity. Moreover, Yu et al. (1999) observed an increase in Cl8:3 in the PM from barley roots (tolerant cultivar) under NaCl stress. The same observation was found for salt tolerant clone buffalo grass (Lin & Wu, 1996), where salt stress caused a greater increase of double bond index which was proposed to be responsible for salt stress tolerance. Under conditions without salt stress, the PM fatty acid composition was already different, unique unsaturated fatty acids were found in salt tolerant buffalo grass clone. This most probable reflects the crucial role of the PM lipids, even in absence of salt stress, in salt acclimation of species/cultivars differing in their response to salinity. Further evidence is provided based on the finding that increasing membrane unsaturated fatty acids in yeast cells, via overexpression of two sunflower oleate [DELTA]12 desaturases, encoded by FAD2-1 and FAD2-3, in yeast cells increased tolerance to high salt (Rodriguez-Vargas et al., 2007). This was due to an increase in the unsaturation index and the fluidity of the yeast membrane. The authors concluded that maintained or increased membrane fluidity is an essential determinant of stress tolerance, and engineering of membrane lipid has the potential to be a useful tool of increasing tolerance to salt stress. In addition, a number of studies report an association between increased PM saturated fatty acids and salt sensitivity. NaCl stress increased saturation of the root PM fatty acids in salt sensitive soybean (Surjus and Durand, 1996). The increase in membrane fatty acid saturation was also greater in salt sensitive com roots (Hajlaoui et al., 2009) and in alga Boekelova hooglandii (Fujii et al., 2001) in response to salinity. Both studies report that one of the primary mechanisms of adaptation to salt stress is linked to the degree of unsaturation of fatty acids in membrane lipids. Lin and Wu (1996) also reported an increase of the PM unsaturated fatty acids in salt tolerant clone of buffalo grass, which was closely related to an increase in membrane permeability. Furthermore, increase in root unsaturation of fatty acids was similarly found in salt tolerant wheat genotypes (Filek et al., 2012). The restructuring of membrane lipid composition has been reported to be one of the adaptations of alga Chlorella vulgaris to survive in high salt concentration, which was mainly achieved by increasing the unsaturation of membrane fatty acids (Lu et al., 2009). The ability of several algae to tolerate high salinity has been shown to be due to increased fatty acid desaturases (Kumari et al., 2013). It is interesting to mention that greater decrease in PM lipid content and fatty acid unsaturation were also correlated with [Al.sup.3+] sensitivity in rice cultivars (Huynh et al., 2012). Based on these results a clear correlation between the PM unsaturated fatty acids and plant tolerance to saline conditions is proposed.
Further evidence supporting the fundamental role of unsaturated fatty acids in plant performance under salinity is the fact that exogenous application of unsaturated fatty acid enhanced plant performance in saline environment. Increased salt tolerance in response to exogenous application of linoleic acid was related to membrane protection and increased activities of the root PM [H.sup.+]-ATPase and [Na.sup.+]/[H.sup.+] antiporter (Zhao & Qin, 2005). On the other hand, exogenous application of palmitic acid (saturated fatty acid) attenuate salt induced injury in root membranes of barley (Zhao & Qin, 2005). Further support is provided by the finding that an increase in the unsaturation of fatty acids in the PM lipids enhances the tolerance to salt stress, which was owing to enhancing the PM [H.sup.+]-ATPase and [Na.sup.+]/[H.sup.+] antiport systems of cyanobacterium Synechococcus (Singh et al., 2002). Azachi et al. (2002) further show that salt adaptation of the alga Dunaliella entailed modifications in the membrane fatty acid composition, involving salt induction of fatty acid elongase jointly with desaturases. This consequently results in a higher ratio of C18 (unsaturated) to Cl6 (saturated) membrane fatty acids. The authors proposed that the activity of the PM [H.sup.+]-ATPase and [Na.sup.+]/[H.sup.+] antiporter was increased by the unsaturation of PM lipids and consequently changing its fluidity. The important role of the PM unsaturated fatty acids in salt tolerance is supported by the data that suppressed activity and synthesis of the [Na.sup.+]/[H.sup.+] antiporter system under high salt conditions is reversed by the unsaturation of fatty acids of the PM (Allakhverdiev et al., 1999). Moreover, unsaturated fatty acids protect membrane against salt-induced damage in Synechococcus (Allakhverdiev et al., 2001). Increased unsaturated fatty acid synthesis under salt stress was in part accounted for tolerance of the salt tolerant wheat cultivar. Extremely high amount of [[DELTA].sup.12] unsaturated fatty acids identified in Chlorella vulgaris in response to salinity leads Lu et al. (2009) to propose involvement of [[DELTA].sup.12] fatty acid desaturase in the process of acclimation to salinity. Ascorbic acid and [alpha]--tocopherol application improved salt tolerance of flax plants, which was also related to increasing unsaturated fatty acids under salt treatment (Sadak & Dawood, 2014). Moreover, the increase in the PM fatty acid saturation in different plant species in response to salinity is believed to correlate with salt sensitivity (Mansour et al., 1994; Kerkeb et al., 2001; Hajlaoui et al., 2009; Mansour, 2013). The previous authors explained that fatty acid saturation correlates with salt sensitivity because fatty acid saturation increases membrane rigidity which modulates transport systems activity and other membrane functions. The mechanism underlying the involvement of the PM unsaturated fatty acids in enhancing plant performance in saline conditions is most likely via their role in maintaining the appropriate membrane fluidity and preservation of the uniform level of its hydration, which ensured the PM stabilization (Leekumjorm et al., 2009). Other investigators (Chalbi et al., 2013; Mansour, 2013) also report that a high level of membrane lipid unsaturation maintains the membrane fluidity necessary for proper membrane functions in various plants. The previous discussion implies clear evidence for the prime role of the PM unsaturated fatty acid in salt adaptation. An increase in unsaturated fatty acids has been evident to stabilize, maintain integrity of the PM, and thus protect cells from salinity injury. We believe that the increase in the PM unsaturated fatty acids to be characteristic of salt tolerance. As far as the more susceptibility of unsaturated fatty acids to oxidative attack is concerned, it appears that salt tolerant plants exhibiting high degree of unsaturation usually have the ability to deal with that through having a greater antioxidant capacity than sensitive ones.
Further support for the crucial role of the PM fatty acids in adaptation to salinity is provided by transgenic plant studies. The mutation that deactivated [DELTA]12 and [DELTA]-6 desaturase drastically inhibited [Na.sup.+]/[H.sup.+] antiport activity of the mutant cells in cyanobacteria Synechocystis sp. PCC 6803 in response to NaCl (Allakhverdiev et al., 1999), suggesting saturation of the PM fatty acids to enhance sensitivity to salt stress. In agreement with that, fatty acid desturase FAD2 was required for salt tolerance in Arabidopsis (Zhang et al., 2012c). Arabidopsis mutant fad2, which lacks the functional FAD2, had lower PM unsaturated fatty acids and reduced PM [Na.sup.+]/[H.sup.+] antiport activity, which resulted in cytoplasmic [Na.sup.+] accumulation and hence salt sensitivity compared with wild type. The results suggest the essentiality of the PM unsaturated fatty acids for proper functioning of [Na.sup.+]/[H.sup.+] antiporter in order to maintain a lower cytosolic [Na.sup.+] and thus enhanced salt tolerance. In accordance, fatty acid desaturase FAD3 has been demonstrated to play a role in increasing drought tolerance of crown galls of Arabidopsis, also via increasing the level of unsaturated fatty acids (Klinkenberg et al., 2014). The fad3-2 mutant with impaired a-linolenic acid synthesis developed significantly smaller crown galls, and had reduced drought stress tolerance. Membranes of Synechococcus sp. transformant with an additional gene of [DELTA]12-acyl-lipid desaturase desA were characterized by an increased level of polyunsaturated fatty acids (Allakhverdiev et al., 2001). Cells of transformant maintained an effective photosynthetic machinery and high activity of [Na.sup.+]/[H.sup.+] antiporters in saline conditions. The authors suggest that enhanced photosynthetic apparatus tolerance to salinity is associated with higher level of membrane fatty acid unsaturation. In a good agreement with the role of fatty acid unsaturation in plant salt tolerance is the finding that overexpression of -3 desaturase increases C18:3 in transgenic tobacco, which improved resistance to salt stress (Zhang et al., 2005). Moreover, Yuan et al. (2014) illustrated that transgenic Arabidopsis producing appreciable amounts of membrane polyunsaturated fatty acids showed enhanced drought resistance. Taken together, the ability of cells to alter the degree of unsaturation in their PM seems to be an important factor in cellular acclimatization to saline conditions.
The PM Glycolipids
Glycolipids are another component of the PM lipids, though they present in even small amount. They are normally associated with the chloroplast. The two predominant species of glycolipids in plants are Monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG). MGDG forms with water a reversed hexagonal phase, while DGDG adopts a lamellar phase. Changes in the ratio of these two molecules thus induce different physical properties in the membranes. The two glycolipids species might therefore play different role in the regulation mechanism under salinity. There are, however, only a limited number of reports on the PM glycolipids changes under salinity stress. The PM glycolipids response to salinity varies in plants differing in salt tolerance, suggesting a possible role in salinity adaptation. Salt treatment had no effect on the PM total glycolipids of barley roots (Brown & DuPont, 1989). Similarly, salt imposition had no significant effect on the PM total glycolipids of salt sensitive wheat roots (Mansour et al., 1994). The PM glycolipids from roots and leaves responded differently in salt tolerant and sensitive cultivars (Bing-Jun et al., 2005; Guimaraes et al., 2011). The glycolipid content in leaves was greater than in roots for both control and salt treated seedlings (Guimaraes et al., 2011). This is expected because of their greater contribution to membranes in photosynthetically active tissues. In response to salt stress, decreases in membrane glycolipids have been observed in wheat and barley leaves (Chetal et al., 1982) and in cowpea leaves (Guimaraes et al., 2011). The PM total glycolipids also decreased in roots of maize cultivars in response to salt treatment, more so in salt tolerant one (Salama et al., 2007). Salt tolerant cultivar has, however, greater PM glycolipid contents relative to the sensitive one in absence of salt stress. Moreover, glycolipid content increased in root membranes of different salt sensitive cultivars, but did not change in the tolerant ones in response to salinity (Huang, 2006). From the results so far, it is obvious that the change in the PM glycolipids is not uniform and varies with species or tissue type. This warrants further intensive research in order to elucidate the glycolipid participation in salt tolerance, and for a conclusion to be drawn.
The PM Proteins and Salt Tolerance
The PM proteomics include structural proteins, anchors, kinases and transport proteins. The involvement of the PM transport proteins in plant adaptation to saline environments have been recently reviewed by Mansour (2014). The response of other PM proteins, collectively we call them PM proteins in general or the PM general proteins, and their relationship to plant adaptation to salt imposition will be only reviewed here. Changes in the proteome of the PM have been reported under saline environment, and are recognized as one of the components involved in tolerance to salinity (Hasegawa et al., 2000). Using proteomics approach, Table 2 shows different identified PM proteins that increased in plants under high salinity. Obviously, identification and characterization of the PM proteins responding to salt stress are important for understanding of salt tolerance in plants. Many studies demonstrated alterations of the PM proteome in plant species/genotypes contrasting in salt sensitivity under saline conditions (Singh et al., 1985; Hurkman et al., 1988, 1989; Kononowicz et al., 1994; Kerkeb et al., 2001; Goncalo et al., 2003; Salama et al., 2007; Katz et al., 2007; Sengupta & Majumder, 2009; Zamani et al., 2010; Zhang et al., 2012b; Huang et al., 2012; Mansour, 2013). These studies report that several of the salt responsive PM proteins produced in salt tolerant species/cultivars improve their salt tolerance, and hence may play an important role in salt acclimation to saline conditions. In addition, Takahashi et al. (2013) recognize alterations in the PM proteomics as a critical adaptation mechanism to abiotic stresses. It can be anticipated that the changes in the PM proteome include qualitative and quantitative differences in plants contrasting in salt tolerance. In agreement with this proposal, Kosova et al. (2013) report that proteins involved in stress response reveal differences in protein structure, activity and level between tolerant plants and sensitive ones. Moreover, salt stress caused greater reduction in the total PM protein concentration of the salt sensitive buffalo grass clone than in the salt tolerant one (Lin & Wu, 1996). Kawasaki et al. (2001) also illustrated increased protein synthesis in rice salt tolerant cultivar under salt imposition, which was suggested to contribute to salt tolerance. The PM proteins of salt tolerant yeast were also increased under NaCl stress, relative to control cells, which was considered as an adaptive response to high salinity (Hosono, 1992). Furthermore, Chang-Qing et al. (2008) demonstrated that salt stress induced two PM protein 3 genes (PutPMP3) from Puccinella tenuiflora, which have been found to be involved in tolerance to salinity. Malakshah et al. (2007) similarly identified eight PM proteins that responded to salt stress. These proteins include 14-3-3 proteins, which are well known as [H.sup.+]-ATPase regulators and also suggested to be involved in pH regulation in cells under salt stress conditions (Babakov et al., 2000). Further supporting is the result of Wang et al. (2014) who report that one upregulated protein under salinity is 14-3-3-like protein, which was also proposed to function as PM [H.sup.+]-ATPase regulator and involved in signal transduction. It is also indicated that salt stress induced 60-kD PM protein in the halotolerance alga Dunaliella, which was hypothesized to play a potential role in salt tolerance through maintaining ion homeostasis under salinity (Fisher et al., 1994). One PM protein that was upregulated under salt stress is cellulose synthase which was proposed to contribute to adaptation of wild halophytic rice to high salinity (Sengupta & Majumder, 2009). When the halophyte Sesuvium portulacastrum treated with high NaCl, 96 salt responsive proteins were produced, the majority of these proteins was involved in ion binding, proton transport, photosynthesis and ATP synthesis, indicating that some of these proteins related to the PM and may be involved in salt adaptation (Yi et al., 2014). Furthermore, the PM of salt-acclimated cyanobacteria, Synechocystis sp. Strain PCC 6803, showed induction of 20 proteins and reduction of five proteins during salt stress (Huang et al., 2006b), which were correlated with salt tolerance.
A number of other PM proteins with different functions were identified in response to high salinity, and thought to be involved in adaptation to salt stress (Hasegawa et al., 2000; Katz et al., 2007; Huang et al., 2012). Among identified proteins in response to salt stress are the PM water channel proteins that might be one of the proteins leading to improvement to salt tolerance. Of 29 different proteins identified in sorghum under NaCl stress, 6.8 % related to lipid metabolism and 6.8 % were proteins involved in signal transduction (Roveda-Hoyos & Fonseca-Moreno, 2011), which may have a role related to the PM properties and functioning. Cheng et al. (2009) identified 18 salt-responsive PM proteins in rice roots. These proteins were involved in membrane stabilization, ion homeostasis, and signal transduction. The receptor proteins identified on the PM are known to sense various environmental stimuli and transduce them to downstream intracellular signaling networks (Cheng et al., 2009). It is important to mention that the receptor proteins located on the PM are suggested as potential candidate genes for genetic engineering of improved stress tolerant crops (Osakabe et al., 2013; Valmonte et al., 2014). On the other hand, overexpression of RPK1 proteins (receptor-like protein kinase) distributed in the PM inhibits Arabidopsis salt tolerance (Shi et al., 2014). Salt tolerance inhibition was attributed to overexpression of RPK1 genes, that down regulated the expression of the SOS3 and P5CS1 (key enzyme in proline synthesis). This leads to SOS signal pathway blocking and proline synthesis inhibition. SOS signal pathway is reported to increase [Na.sup.+] efflux and hence ion homeostasis under high salinity. SOS signal pathway blocking therefore increased [Na.sup.+] accumulation in the transgenic Arabidopsis plants and inhibited its tolerance. However, inhibition of the expression of the atRPKl gene in Arabidopsis improved salt tolerance. Overexpression of Medicago sativa stress-induced MAPKK (SIMKK)SIMK in Arabidopsis also exhibited high salt sensitivity (Ovecka et al., 2014). Increased salt sensitivity of the transgenic plants has been found to be consistent with their proteome composition. It appears that the PM receptor proteins overexpression under salt stress, function primarily in signaling cascades, may not always act in a favorable direction for stress tolerance. In addition, some of protein partners (in the previous study MPK3/MPK6) that make up the signaling pathways may disrupt other useful pathways or hijack the salt response pathway resulting in increased salt sensitivity. Moreover, overexpression of salt stress-induced glycine-rich protein gene (MsGRP) from alfalfa causes salt sensitivity in Arabidopsis (Long et al., 2013). This MsGRP protein is localized in the PM, and has been indicated to play a critical role in salt stress regulation. A proposed function for this salt-induced protein is that it probably plays a role in the porins on the PM and participates in water transport (Long et al., 2013). It is also important to mention that not all proteins produced in saline conditions are correlated with stress tolerance. A cross between two salt sensitive wheat cultivars and highly salt tolerant Elytrigia elongata produced two cultivars tolerant to high salt (Roy & Gurjar, 1997). However, salt stress affected twice as many genes in one cultivar than in the other suggesting that a number of genes which are affected by salt stress may have little or nothing to do with the control of salt tolerance (Roy & Gurjar, 1997). Sobhanian et al. (2011) similarly demonstrate that some of the salt response proteins are probably part of a general stress response and may not related to salt tolerance. Other reports indicate also that polypeptide pattern of the PM from wheat sensitive and tolerant roots (Mansour et al., 1998, 2000) and from sugar beet roots (Yahya et al., 1995) did not change significantly under salinity. The PM total proteins from roots of canola tolerant and sensitive cultivars did not also significantly change in response to salt imposition (Zamani et al., 2010). Moreover, the PM total proteins of the halophyte Spartina patens callus was decreased in response to NaCl stress (Wu et al, 2005). This apparent discrepancy could be attributed to the fact that not all salt responsive proteins related to salinity adaptation, and may be merely a detrimental effect of salinity. The role of salt stress related PM proteins in adaptation to saline conditions is, however, evident and cannot be ruled out.
Further evidence emphasizes the prime role of the PM proteins in salt tolerance is provided by the finding that overexpression of AtLTL1 (Li-tolerant lipase 1), a salt-induced gene encoding a GDSL-motif lipase, increases salt tolerance in transgenic Arabidopsis plants (Naranjo et al., 2006). AtLTL1 is a protein anchored to the PM, and has been suggested to act by releasing fatty acids from membrane lipids. The importance of this protein comes from the fact that fatty acids are essential signaling molecules in plants that are involved in mechanisms of defense against biotic and abiotic stresses (Naranjo et al., 2006). In addition, overexpression of a novel dehydrin gene, MusaDHN-1, contributes affirmatively to salt stress tolerance in banana (Shekhawat et al., 2011). Dehydrin has been reported to present in vicinity of the PM (Rorat, 2006), bind and protect membranes, and also protect against oxidative stress under stresses (Graether & Boddington, 2014). Abscisic acid-activated protein kinase (AAPK), with sequence homology to heterogenous nuclear RBP (RNA-binding proteins), has been shown to regulate the PM ion channels (Li et al., 2002). The study also reports that this protein is required for interaction with mRNA encoding dehydrin. In the same line, a recent study demonstrates that RBP is an environmentally regulated protein in response to salt stress (Lee et al., 2014). Furthermore, overexpressing ubiquitin, a stress protein, promoted salt tolerance of transgenic tobacco (Zhang et al., 2012a). The authors proposed changes in antioxidant capacity to be one of the mechanisms underlying ubiquitin regulation of salt tolerance. Elevated antioxidant capacity implies ubiquitin role in protection of the PM lipids. Further evidence is provided that salt responsive proteins may indirectly modulate the PM contribution to salt tolerance. This is based on fact that salinity-induced alterations in protein biosynthesis related to lipid metabolism leads to profound changes in PM lipid composition and hence its integrity and function under saline conditions (Kosova et al., 2013). Another PM protein that when overexpressed in Arabidopsis and Cochlearia hollandica confers salt tolerance is the PM [Na.sup.+]/[H.sup.+] antiporter, which its activity and expression increase under salinity in salt tolerant plants (Mansour, 2014; Nawaz et al., 2014). Moreover, overexpression of the rice PM intrinsic protein gene (OsPIP) in wild type Arabidopsis enhanced tolerance to 100 mM NaCl (Guo et al., 2006), suggesting a distinct role of OsPIP gene in response to salt stress. Overexpression of GmPIPl;6 similarly increased salt tolerance of soybean by improving root water absorption and [Na.sup.+] exclusion (Zhou et al., 2014). It is worth noting that both OsPIP and GmPIP1;6 are PM intrinsic proteins involved in water absorption needed for cell extension. Further supporting evidence is that salt-induced proteins involved in ROS detoxification will minimize the PM lipid peroxidation and thus participate in the PM integrity maintenance, and thus functioning properly during salinity stress. The salt-induced proteins participating in ROS detoxification were identified as potential candidates for increasing salt tolerance in barley (Witzel et al., 2009). Owing to the importance of the salt-responsive PM proteins in salt stress response, it is reported that one strategy to increase the level of salinity tolerance is the transfer of genes codifying different types of proteins functionally related to macromolecules protection (Amudha & Balasubramani, 2011; Munoz-Mayor et al., 2012). The aforementioned discussion implies clear evidence for the involvement of salt-responsive PM proteins in adaptation to salinity.
Published reports addressed the functions of the PM proteins induced under salt stress. Different works demonstrate that salinity-induced PM proteins in the salt tolerant species/cultivars may have protective functions against the negative effects of salt stress. One of the salt-induced PM protective proteins that produced in different tolerant genotypes under salinity is 29 KDa protein (osmotin) (Hurkman et al., 1988; Kononowicz et al., 1994; Salama et al., 2007). Osmotin is also identified as a key protein in salt tolerance of the mangrove plant Bruguiera gymnorhiza (Tada & Kashimura, 2009). Osmotin is hypothesized to regulate plant responses to different environmental stresses through its involvement as an osmoprotectant and a cell signal pathway modulator (Abdin et al., 2011). It is also shown that overexpression of tobacco osmotin gene enhances strawberry salt tolerance (Husaini & Abdin, 2008), further support for the involvement of salt-responsive proteins in salt tolerance mechanism. Another possible role of salinity-induced changes in the PM polypeptides is that these new proteins may modulate specific molecular interactions between lipids and proteins, and between proteins themselves (Simon, 1974; Russell, 1989; Russell et al., 1995; Sorek et al., 2009; Mansour, 2013). Such effects play diverse roles in subcellular targeting, protein-protein interactions and signaling (Sorek et al., 2009), thus regulating the PM transport systems and hence plant ion homeostasis under saline conditions (Amtmann & Beilby, 2010). Some of the PM responsive proteins have been found to participate in signal transduction since PM receptor proteins were higher in abundance in response to saline environments (Ghosh & Xu, 2014). Of 55 identified proteins in the PM of the halotolerant alga Dunaliella salina under high salinity, about 60 % were integral membrane proteins, implicated in protein and membrane structure stabilization as well as within signal transduction pathways (Katz et al., 2007). Malakshah et al. (2007) also report that the membrane proteins responding to stresses may have roles in the repair and protection of the PM as well as signal transduction. In addition, a 150 KDa PM localized protein was induced by salt in the halophyte alga Dunaliella salina (Sadka et al., 1991), a role related to permeability or flux properties of the PM was proposed. Regulatory and protective functions of proteins elevated in response to saline environment have been presented. One protein upregulated in wheat under salt stress has been found to alleviate salinity effects by regulating the PM [H.sup.+]-ATPase and hence maintaining ion homeostasis (Wang et al., 2008b). Moreover, three homologues of soybean PM [H.sup.+]-ATPase and calnexin (a molecular chaperon protein) were upregulated under osmotic stress (Nouri & Komatsu, 2010). The chaperone protein calnexin accumulates in the PM and characterized by assisting protein folding. Similarly, salt stress induced the PM [H.sup.+]-ATPases and ABC transporters upregulation in the leaves of mangrove plant (Krishnamurthy et al, 2014). ATPases function as energy source for secondary [Na.sup.+] exclusion, and ABC transporters are involved in ion detoxification (Mansour, 2014; Krishnamurthy et al., 2014), a feature greatly contributes to salt tolerance. The protein pattern of the PM from salt adapted cells of the cyanobacterium Anacystis nidulans also showed the appearance of new bands in saline environment, which stem from the PM [Na.sup.+]/[H.sup.+] antiporter (Molitor et al., 1990). This results in enhancing the activity of the PM [Na.sup.+]/[H.sup.+] antiporter of salt adapted cells; [Na.sup.+]/[H.sup.+] antiporters are known to play a key role in [Na.sup.+] exclusion under high salt. Vialaret et al. (2014) identified PM proteins from Arabidopsis roots that upregulated in response to NaCl treatment. These proteins include PM transport proteins and protein kinases, which are involved in ion homeostasis and signal perception. The authors also demonstrate that the PM proteins are the target of different protein kinases in response to NaCl stress, and also point out to an important role for lipid signaling in salt stress responses in plants. Other PM proteins that have been shown to be upregulated under salt stress, and correlate with salt tolerance are aquaporins (Mansour, 2014, Vialaret et al., 2014). Aquaporins are mainly involved in water absorption under salinity. Briefly, functions of the PM related salt-responsive proteins may involve scavenging of ROS, signal transduction, lipid metabolism and protection, regulation, membrane and transport (Zhang et al., 2012b; Huang et al., 2012; Ghaffari et al., 2014). Taken together, it seems that salt-responsive proteins may protect or induce synthesis of protective molecules that stabilize the PM integrity and hence maintain its proper functionality under high salinity. It can be also inferred that these proteins most likely involved in alleviating the negative effects of salt stress through retaining the activities of ion transport systems and ion homeostasis, and thus induce salt tolerance. Despite the fact that several PM salt responsive proteins play a defined adaptive role in response to salt stress, the function of others still remains obscure.
Conclusions and Future Perspectives
As the PM is the cell part that salt reaches first, numerous studies therefore suggest the PM as the first target of high salinity injury. It is thus believed that the PM might play a fundamental role in adaptation to high salinity. This contention is based on the fact that the PM lipids and proteins are the most important agents regulating ion homeostasis under salinity. In addition, the PM components have also a pivotal role in cellular signal transduction under salt stress, and salinity stress is thought to be perceived at the PM. Evidence is also provided that the responses of the PM lipids and proteins are different in plant species/ cultivars contrasting in salt tolerance under saline conditions. It is thus reasonable to believe that the primary mechanism by which salt affects sensitive plant functioning is through disturbance of the PM composition and properties. Even though we are still at an early stage in understanding the involvement of PM components at molecular level in plant adaptation to salinity, many studies indicate that PM qualitative and quantitative adjustments could be a mechanism decisively contributing to salt tolerance. In this respect, it is proposed that specific alteration in individual molecular species of the PM lipids may work in tandem with others and/or may be counteracted by other lipid changes, which may ultimately aggravate (i.e., sensitive plants) or minimize (i.e., tolerant plants) the deleterious effects of salinity on the PM stability and functioning. It is consequently believed that salt tolerant plants could better preserve the composition/ structure of their PM and thus the cells integrity, a feature that allows them to maintain a better growth under salinity. In light of the above, we suggest the PM components to be one of the salt adaptation mechanisms in plants. It is important to mention, however, that information on some issues of the PM components involvement in salt adaptation is not conclusive and more detailed studies are necessary for a full understanding of their contribution to plant salt tolerance. Moreover, the possible links between PM component alterations and salt tolerance must be also interpreted carefully, since biological membranes are extremely complex structures consisting of hundreds of different lipid and protein molecules, which may lead to a various regulation mechanisms under different stress conditions. It will be hence crucial for future research studies on responses of the PM to salinity to elucidate the molecular mechanisms that link the PM individual lipids and proteins to salt tolerance. We need also a better understanding of the PM proteome under salt stress. These approaches would help in developing strategies to enhance tolerance to salinity. Furthermore, as exposure to salinity activates a gene or a set of genes that are responsible for specific molecular lipid and/or protein formation, overexpression of enzymes that affect one membrane lipid or protein species that modulate tolerance to salinity is a promising area for future research.
DOI 10.1007/s 12229-015-91564
Published online: 21 July 2015
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Mohamed Magdy F. Mansour (1,2,4,1,2) * Karima H. A. Salama (2,2) * Hasan Y. H. Allam (1,3)
(1) Department of Biology, Faculty of Science, Taif University, Taif 21944, Saudi Arabia
(2) Department of Botany, Faculty of Science, Ain Shams University, Cairo 11566, Egypt
(3) Faculty of Agriculture, Al-Azhar University, Cairo 11884, Egypt
(4) Author for Correspondence; e-mail: firstname.lastname@example.org
Table 1 Plasma membrane lipid classes that contributing to adaptation to saline conditions from different plant species Species Rating Tissue Lipid class Phospholipids Triticum aestivum Sensitive Root PC Plantago sp. Tolerant Root PC Spartina patens Halophyte Callus PC Solatium lycopersicum Sensitive Root PC Brassica napus Tolerant Root PG Zea mays Tolerant Root PG Bouteloua dactyloides Tolerant Root PG Zea mays Tolerant Root PE Bouteloua dactyloides Tolerant Root PE Zea mays Sensitive Root PI Triticum aestivum Sensitive Root PI Solanum lycopersicum Sensitive Root PI Brassica napus Sensitive Root PI Sterols Spartina patens Halophyte Callus Campesterol Spartina patens Halophyte Callus Sitosterol Solanum lycopersicum Tolerant Callus Campesterol Triticum aestivum Sensitive Root Stigmastcrol Citrus sinensis Tolerant Root Stigmasterol Citrus sinensis Sensitive Root Campesterol Citrus sinensis Tolerant Root Sitosterol Brassica oleracea Tolerant Root Stigmasterol Brassica oleracea Tolerant Root Sitosterol Hordeum vulgare Tolerant Root Stigmastcrol Hordeum vulgare Tolerant Root Sitosterol Fatty acids Triticum aestivum Sensitive Root 18:3 Zea mays Tolerant Root 18:3 Zea mays Tolerant Root 25:5 Bouteloua dactybides Tolerant Root 18:3 Bouteloua dactybides Sensitive Root 18:3 Hordeum vulgare Tolerant Root 18:3 Zea mays Sensitive Root 18:2 Species Response Reference Phospholipids Triticum aestivum Decrease Mansour et al. (1994) Plantago sp. Increase Kuiper (1984) Spartina patens No effect Wu et al. (2005) Solatium lycopersicum Decrease Racagni et al. (2003) Brassica napus Increase Zamani et al. (2010) Zea mays Increase Salama et al. (2007) Bouteloua dactyloides Increase Lin and Wu (1996) Zea mays Decrease Salama et al. (2007) Bouteloua dactyloides Decrease Lin and Wu (1996) Zea mays Increase Salama et al. (2007) Triticum aestivum Increase Mansour et al. (1994) Solanum lycopersicum Increase Racagni et al. (2003) Brassica napus Increase Zamani et al. (2010) Sterols Spartina patens Increase Wu et al. (2005) Spartina patens Decrease Wu et al. (2005) Solanum lycopersicum Increase Kerkeb et al. (2001) Triticum aestivum Increase Mansour et al. (1994) Citrus sinensis Increase Douglas (1985) Citrus sinensis Decrease Douglas (1985) Citrus sinensis Decrease Douglas (1985) Brassica oleracea Increase Lopez-Perez et al. (2009) Brassica oleracea Decrease Lopez-Perez et al. (2009) Hordeum vulgare Increase Brown and DuPont (1989) Hordeum vulgare Decrease Brown and DuPont (1989) Fatty acids Triticum aestivum Decrease Mansour et al. (1994) Zea mays Increase Hajlaoui et al. (2009) Zea mays Increase Hajlaoui et al. (2009) Bouteloua dactybides Increase Lin and Wu (1996) Bouteloua dactybides Decrease Lin and Wu (1996) Hordeum vulgare Increase Yu et al. (1999) Zea mays Decrease Salama et al. (2007) Table 2 Identified plasma membrane (PM) proteins increased in plants under salt stress using proteomics approach Plant Identified protein Arabidopsis thaliana [Na.sup.+]/[H.sup.+] antiporter Cochlearia hollandica [Na.sup.+]/[H.sup.+] antiporter Dunaliella salina 60-KD protein Porteresia coarctata Cellulose synthase Puccinella tenuiflora PutPMP3 Oryza saliva 14-3-3 protein Oryza sativa OsRPKl Fragaria ananassa Osmotin Glycine max GmPIPl;6 Dunaliella salina 150-KD protein Triticum aestivum 14-3-3 protein Arabidopsis thaliana AtLTLI Musa paradisiaca Dchydrin Cldorella vulgaris CvFAD2 Avicennia officinalis ABC transporters Kandelia candel 14-3-3-like protein Oryza sativa Protein kinases Avicennia officinalis [H.sup.+]-ATPases Plant Role of the protein in salt tolerance Arabidopsis thaliana [Na.sup.+] extrusion Cochlearia hollandica [Na.sup.+] extrusion Dunaliella salina Ion homeostasis Porteresia coarctata Cell wall synthesis Puccinella tenuiflora PM hypcrpolarization reserving Oryza saliva [H.sup.+]-ATPase regulator Oryza sativa Signal transduction Fragaria ananassa PM protectant Glycine max Water transporter Dunaliella salina PM permeability Triticum aestivum [H.sup.+]-ATPase regulator Arabidopsis thaliana Releasing fatty acids from PM Musa paradisiaca PM protectant Chlorella vulgaris Fatty acid unsaturation Avicennia officinalis Ion detoxification Kandelia candel [H.sup.+]-ATPase regulator Oryza sativa Signal transduction Avicennia officinalis Energy source for secondary ion transporter Plant Reference Arabidopsis thaliana Mansour (2014) Cochlearia hollandica Nawaz et al. (2014) Dunaliella salina Fisher et al. (1994) Porteresia coarctata Sengupta and Majumder (2009) Puccinella tenuiflora Chang-Qing et al. (2008) Oryza saliva Malakshah et al. (2007) Oryza sativa Cheng et al. (2009) Fragaria ananassa Husaini and Abdin (2008) Glycine max Zhou et al. (2014) Dunaliella salina Sadka et al. (1991) Triticum aestivum Wang et al. (2008b) Arabidopsis thaliana Naranjo et al. (2006) Musa paradisiaca Shekhawat et al. (2011) Chlorella vulgaris Lu et al. (2009) Avicennia officinalis Krishnamurthy et al. (2014) Kandelia candel Wang et al. (2014) Oryza sativa Vialaret et al. (2014) Avicennia officinalis Krishnamurthy et al. (2014) s
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|Author:||Mansour, Mohamed Magdy F.; Salama, Karima H.A.; Allam, Hasan Y.H.|
|Publication:||The Botanical Review|
|Date:||Dec 1, 2015|
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