Protection of Plasma Membrane K+ Transport by the Salt Overly Sensitive1 Na+-H+ Antiporter during Salinity Stress

Abstract

Physicochemical similarities between K+ and Na+ result in interactions between their homeostatic mechanisms. The physiological interactions between these two ions was investigated by examining aspects of K+ nutrition in the Arabidopsis salt overly sensitive (sos) mutants, and salt sensitivity in the K+ transport mutants akt1 (Arabidopsis K+ transporter) and skor (shaker-like K+ outward-rectifying channel). The K+-uptake ability (membrane permeability) of the sos mutant root cells measured electrophysiologically was normal in control conditions. Also, growth rates of these mutants in Na+-free media displayed wild-type K+ dependence. However, mild salt stress (50 mm NaCl) strongly inhibited root-cell K+ permeability and growth rate in K+-limiting conditions of sos1 but not wild-type plants. Increasing K+ availability partially rescued the sos1 growth phenotype. Therefore, it appears that in the presence of Na+, the SOS1 Na+-H+ antiporter is necessary for protecting the K+ permeability on which growth depends. The hypothesis that the elevated cytoplasmic Na+ levels predicted to result from loss of SOS1 function impaired the K+ permeability was tested by introducing 10 mm NaCl into the cytoplasm of a patch-clamped wild-type root cell. Complete loss of AKT1 K+ channel activity ensued. AKT1 is apparently a target of salt stress in sos1 plants, resulting in poor growth due to impaired K+ uptake. Complementary studies showed that akt1 seedlings were salt sensitive during early seedling development, but skor seedlings were normal. Thus, the effect of Na+ on K+ transport is probably more important at the uptake stage than at the xylem loading stage.

Sodium as nutrient and toxicant

“…Moreover, transcript abundances of both KUP/HAK/KT transporters (Su et al 2002;Nieves-Cordones et al 2007) and Shaker-type K + channels (Su et al 2001;Golldack et al 2003;Pilot et al 2003) can be affected negatively by NaCl. In most cases, transport inhibition is believed to be mediated by Na + binding to the outside of carriers and channels , although, in the case of some Shaker-type channels, a mechanism has also been proposed whereby small concentrations of cytosolic Na + (near 10 mM) can effect inhibition from the inside of the cell (Qi and Spalding 2004); such concentrations are considered easily attained (Carden et al 2003;Kronzucker and Britto 2011). In addition, as pointed out previously, K + efflux via outward-rectifying channels has been shown to be stimulated by Na + -induced depolarization of the plasma membrane (Shabala et al 2006; Fig.…”

“…Figure 1 summarizes the key events that are expected to lead to compromised cytosolic K + homeostasis in typical root cells. Na + can directly inhibit high-affinity K + transporters of the KUP/HAK/KT family (SantaMaría et al 1997;Quintero and Blatt 1997;Fu and Luan 1998;Senn et al 2001) and Shaker-type K + channels (Thiel and Blatt 1991;Qi and Spalding 2004;Fuchs et al 2005;Wang et al 2007). Moreover, transcript abundances of both KUP/HAK/KT transporters (Su et al 2002;Nieves-Cordones et al 2007) and Shaker-type K + channels (Su et al 2001;Golldack et al 2003;Pilot et al 2003) can be affected negatively by NaCl.…”

Rice Shaker Potassium Channel OsKAT1 Confers Tolerance to Salinity Stress on Yeast and Rice Cells

“…AKT1 is an inward-rectifying channel for K 1 uptake in Arabidopsis roots. Elevated cytoplasmic Na 1 impaired the K 1 permeability mediated by AKT1 (Qi and Spalding, 2004). OsAKT1 is also reported to represent the dominant salt-sensitive K 1 uptake channel in rice roots (Fuchs et al, 2005), and the expression of OsAKT1 is regulated differently in salt-sensitive and salt-tolerant cultivars of rice (Golldack et al, 2003).…”

Activation of the plasma membrane Na/H antiporter Salt-Overly-Sensitive 1 (SOS1) by phosphorylation of an auto-inhibitory C-terminal domain

“…SOS1 is thought to mediate Na efflux at the root epidermis and longdistance transport from roots to shoots (4, 6) while protecting individual cells from Na toxicity (7-9). SOS1 is also indirectly required for the uptake of potassium (K) in the presence of Na, although the mechanistic basis is not fully understood (7,8,10). Both the protein kinase SOS2 and its associated calcium-sensor subunit SOS3 are required for the posttranslational activation of SOS1 Na/H exchange activity in Arabidopsis (11,12), and a similar regulatory module operates also in cereals (13).…”