Regulation of Na+ and K+ homeostasis in plants: towards improved salt stress tolerance in crop plants

Abstract

Soil salinity is a major abiotic stress that results in considerable crop yield losses worldwide. However, some plant genotypes show a high tolerance to soil salinity, as they manage to maintain a high K+/Na+ ratio in the cytosol, in contrast to salt stress susceptible genotypes. Although, different plant genotypes show different salt tolerance mechanisms, they all rely on the regulation and function of K+ and Na+ transporters and H+ pumps, which generate the driving force for K+ and Na+ transport. In this review we will introduce salt stress responses in plants and summarize the current knowledge about the most important ion transporters that facilitate intra- and intercellular K+ and Na+ homeostasis in these organisms. We will describe and discuss the regulation and function of the H+-ATPases, H+-PPases, SOS1, HKTs, and NHXs, including the specific tissues where they work and their response to salt stress.

Figure 1. Schematic representation showing key plasma and tonoplast membrane transporters, channels and pumps mediating Na⁺ and K⁺ homeostasis in plants under salt stress (adapted from Roy et al., 2014). Na⁺ ions enter the cells via Non Selective Cation Channels (NSCCs) and possibly via other cation transporters not shown (symplast flow - blue arrow) and through the cell wall and intercellular spaces (apoplast flow - red arrow). The Na⁺/H⁺ antiporter SOS1 extrudes Na⁺ at the root soil interface, thus reducing the Na⁺ net influx of Na⁺. At the xylem parenchyma cells, HKT1-like proteins retrieve Na⁺ from the xylem sap, thereby restricting the amount of Na⁺ reaching the photosynthetic tissues. To translocate Na⁺ back to the root, ions unloaded from xylem may be transported into phloem via additional HKT1-like protein. In addition, HKT1-like proteins also load Na⁺ into shoot phloem, and then Na⁺ is transferred into roots via phloem, preventing Na⁺ accumulation in shoots. SOS1, localized in the xylem parenchyma cells, is also suggested to mediate Na⁺ efflux from xylem vessels under high salinity. Incoming Na⁺, in root and shoots, is stored in the large central vacuole by tonoplast-localized NHX exchangers (NHX1-4). Plasma membrane (PM) H⁺-ATPase (P-ATPase), PM H⁺-PPase (PM-PPase), tonoplast H⁺-ATPase (V-ATPase) and tonoplast H⁺-PPase (V-PPase) generate electrochemical potential gradient for secondary active transport.

Figure 2. Schematic representation of a hypothetical Arabidopsis cell indicating subcellular localizations, functions, and regulations of NHXs antiporters (NHX1-6), plasma membrane H⁺-ATPase (P-ATPase), tonoplast H⁺-ATPase (V-ATPase), tonoplast H⁺-PPase (V-PPase) and SOS1 (adapted from Bassil et al., 2012). Trans-Golgi network (TGN), and prevacuolar compartment (PVC).

Figure 3. Structural model of the plant V-ATPase adapted from Gaxiola et al. (2007). The peripheral V₁ complex (blue) and the membrane integral V₀ complex (orange) are linked through a peripheral stalk formed by subunits a, C, E, G and H. Hydrolysis of ATP is coupled with H⁺ transport to the vacuole.