A pharmacological analysis of high-affinity sodium transport in barley (Hordeum vulgare L.): a 24Na+/42K+ study

Abstract

Soil sodium, while toxic to most plants at high concentrations, can be beneficial at low concentrations, particularly when potassium is limiting. However, little is known about Na+ uptake in this ‘high-affinity’ range. New information is provided here with an insight into the transport characteristics, mechanism, and ecological significance of this phenomenon. High-affinity Na+ and K+ fluxes were investigated using the short-lived radiotracers 24Na and 42K, under an extensive range of measuring conditions (variations in external sodium, and in nutritional and pharmacological agents). This work was supported by electrophysiological, compartmental, and growth analyses. Na+ uptake was extremely sensitive to all treatments, displaying properties of high-affinity K+ transporters, K+ channels, animal Na+ channels, and non-selective cation channels. K+, NH4+NH4+, and Ca2+ suppressed Na+ transport biphasically, yielding IC50 values of 30, 10, and <5 μM, respectively. Reciprocal experiments showed that K+ influx is neither inhibited nor stimulated by Na+. Sodium efflux constituted 65% of influx, indicating a futile cycle. The thermodynamic feasibility of passive channel mediation is supported by compartmentation and electrophysiological data. Our study complements recent advances in the molecular biology of high-affinity Na+ transport by uncovering new physiological foundations for this transport phenomenon, while questioning its ecological relevance.

Sodium efflux in plant roots: What do we really know?

“…This includes most of the early work in this area, whichfocused on Na + transport at ~1 mM [Na + ] ext or less. In this concentration range, pronounced stimulation and inhibition of Na + release from radiolabeled plant tissues have been frequently observed in reaction to many experimental treatments including ouabain (Davis and Jaworski, 1979), fusicoccin (Marrè, 1979), abscisic acid (Behl and Jeschke, 1981), changes in external pH (Behl and Raschke, 1986;Jacoby and Teomy, 1988;Mennen et al, 1990), changes in temperature (Nassery and Baker, 1972b;Macklon, 1975), and changes in external K + supply (Jeschke, 1983;Schulze et al, 2012).…”

Sodium as nutrient and toxicant

“…If Na + can be readily beneficial in so many plant species and, associated with this, accumulate to significant concentrations in plant organelles and organs to levels similar to those of K + (Gattward et al 2012;Schulze et al 2012), there must be efficient pathways for its entry across root plasma membranes. Interestingly, despite considerable effort, entry paths for Na + into roots have not as yet been successfully identified at the molecular level across taxonomic groups (Munns and Tester 2008;Zhang et al 2010;Kronzucker and Britto 2011;Cheeseman 2013), while a strong body of evidence has shown, at least in grasses, that one family of genes, HKT2 (formerly referred to as HKT1, but the latter designation is now reserved for a group of Na + transporters believed to be predominantly involved in intra-plant Na + transfer from root to shoot; Sunarpi et al 2005;Møller et al 2009), encodes transporters that can transport Na + at substantial rates across root plasma membranes, especially when K + is limiting (Horie et al 2001(Horie et al , 2011Laurie et al 2002;Munns and Tester 2008;Hauser and Horie 2010).…”

“…However, only very limited (and misleading; see Haro et al 2005) demonstrations of such a function outside heterologous expression systems, such as Xenopus oocytes and yeast cells, have thus far occurred (Rubio et al 1995;Spalding et al 1999;Haro et al 2005). Other than these instances, little evidence for Na + -coupled K + uptake exists in terrestrial plants Rodríguez-Navarro and Rubio 2006;Corratgé-Faillie et al 2010;Schulze et al 2012), although it may play a significant role in aquatic angiosperms and algae . A far more common observation is that Na + , at already modest (below-saline) concentrations, inhibits K + -influx systems, both in the high-and low-affinity transport ranges for K + (Rains and Epstein 1967a, b, c;Cheeseman 1982;Jeschke 1982;Kochian et al 1985;Benlloch et al 1994;Schachtman and Schroeder 1994;Santa-María et al 1997;Flowers and Hajibagheri 2001;Fuchs et al 2005;Martínez-Cordero et al 2005;Kronzucker et al 2006Kronzucker et al , 2008Nieves-Cordones et al 2007;Wang et al 2007), and can, additionally, stimulate K + efflux (Shabala et al 2006;Britto et al 2010;Coskun et al 2013), thus depressing K + -utilization efficiency in a two-pronged fashion.…”

“…Those from the HKT1 subfamily are believed to operate mostly in regulating root-to-shoot Na + translocation (Sunarpi et al 2005;Møller et al 2009), while those from the HKT2 subfamily have been implicated in primary Na + influx at least at lower Na + concentrations and in grasses (Horie et al 2001;Laurie et al 2002;Munns and Tester 2008;Hauser and Horie 2010;Horie et al 2011; see also Schulze et al 2012). In addition, two Na + /H + antiport systems have been identified, one of which, SOS1, is believed to be responsible predominantly for Na + efflux at the plasma membrane (Shi et al 2000), the other, NHX1, for Na + sequestration into the vacuole (Apse et al 1999).…”

Plant High-Affinity Potassium (HKT) Transporters Involved in Salinity Tolerance: Structural Insights to Probe Differences in Ion Selectivity

“…This uncertainty is compounded by paucity of direct evidence showing Na + /K + symport in wheat [61], barley [62] and rice [63] roots, calling into question the putative role of HKT2-type proteins in plants in the uptake of K + , in K + deficient conditions, using the electrochemical gradient for Na + [57,64]. This means that either the results from heterologous systems are incorrect or the activity of the HKTs in planta has been masked in these particular experiments through the activity of other plant proteins or in the specific conditions imposed.…”