Non-reciprocal interactions between K+ and Na+ ions in barley (Hordeum vulgare L.)

Abstract

The interaction of sodium and potassium ions in the context of the primary entry of Na+ into plant cells, and the subsequent development of sodium toxicity, has been the subject of much recent attention. In the present study, the technique of compartmental analysis with the radiotracers 42K+ and 24Na+ was applied in intact seedlings of barley (Hordeum vulgare L.) to test the hypothesis that elevated levels of K+ in the growth medium will reduce both rapid, futile Na+ cycling at the plasma membrane, and Na+ build-up in the cytosol of root cells, under saline conditions (100 mM NaCl). We reject this hypothesis, showing that, over a wide (400-fold) range of K+ supply, K+ neither reduces the primary fluxes of Na+ at the root plasma membrane nor suppresses Na+ accumulation in the cytosol. By contrast, 100 mM NaCl suppressed the cytosolic K+ pool by 47–73%, and also substantially decreased low-affinity K+ transport across the plasma membrane. We confirm that the cytosolic [K+]:[Na+] ratio is a poor predictor of growth performance under saline conditions, while a good correlation is seen between growth and the tissue ratios of the two ions. The data provide insight into the mechanisms that mediate the toxic influx of sodium across the root plasma membrane under salinity stress, demonstrating that, in the glycophyte barley, K+ and Na+ are unlikely to share a common low-affinity pathway for entry into the plant cell.

Mechanisms of sodium uptake by roots of higher plants

“…Above that concentration, a suppression of Na + fluxes only by 50 mM K + was found (Wang et al 2007), indicating, in Suaeda, the reciprocal effect of K + on Na + influx exists only under high K + (50 mM) and high Na + (above 100 mM) conditions. At 100 mM external [Na + ], a 27-fold variation in K + (1.5-40 mM) supply resulted in no significant differences in influx, efflux, or net flux of sodium in barley Kronzucker et al 2008). Previous work on the interactions between these ions also showed no significant differences in [Na + ] cyt between 0.1 mM and 1.5 mM external [K + ] with increasing external [Na + ] (1-100 mM) (Kronzucker et al 2006).…”

Sodium as nutrient and toxicant

“…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.…”

“…The potassium target A large number of studies has shown the disruption of both cellular and whole-plant potassium homeostasis under sodium stress (Rains and Epstein 1967a, b, c;Flowers and Läuchli 1983;Watad et al 1991;Gaxiola et al 1992;Warne et al 1996;Zhu et al 1998 Takahashi et al 2007;Kronzucker et al 2008;Britto et al 2010;Coskun et al 2013, cf. Seemann andCritchley 1985).…”

“…1) and is attributable to sodium's effects on K + transport Kronzucker and Britto 2011). Na + has been shown to suppress K + influx in both its high-and low-affinity ranges, particularly at millimolar concentrations (Cheeseman 1982;Jeschke 1982;Schachtman and Schroeder 1994;Rubio et al 1995;Gassmann et al 1996;Maathuis et al 1996;Santa-María et al 1997;Martínez-Cordero et al 2005;Kronzucker et al 2006Kronzucker et al , 2008Nieves-Cordones et al 2007). Some studies have reported only weak Na + effects (Epstein 1961;Epstein et al 1963; see also Seemann and Critchley 1985), or even stimulations of K + influx by Na + (Rubio et al 1995;Spalding et al 1999), but such studies are in the minority.…”

The Role of Ion Channels in Plant Salt Tolerance

“…This system seems to be similarly crucial in salt-sensitive and salttolerant species (Oh et al 2007). Futile cycling occurs to a varying degree in all plants investigated so far with 78-98% of Na + taken up transported back into the environment (Kronzucker et al , 2008Wang et al 2006Wang et al , 2009Malagoli et al 2008). A second strategy for removing Na + from the cytoplasm is to compartmentalise it in the vacuoles.…”