K+ Efflux and Retention in Response to NaCl Stress Do Not Predict Salt Tolerance in Contrasting Genotypes of Rice (Oryza sativa L.)

Abstract

Sudden elevations in external sodium chloride (NaCl) accelerate potassium (K+) efflux across the plasma membrane of plant root cells. It has been proposed that the extent of this acceleration can predict salt tolerance among contrasting cultivars. However, this proposal has not been considered in the context of plant nutritional history, nor has it been explored in rice (Oryza sativa L.), which stands among the world’s most important and salt-sensitive crop species. Using efflux analysis with 42K, coupled with growth and tissue K+ analyses, we examined the short- and long-term effects of NaCl exposure to plant performance within a nutritional matrix that significantly altered tissue-K+ set points in three rice cultivars that differ in salt tolerance: IR29 (sensitive), IR72 (moderate), and Pokkali (tolerant). We show that total short-term K+ release from roots in response to NaCl stress is small (no more than 26% over 45 min) in rice. Despite strong varietal differences, the extent of efflux is shown to be a poor predictor of plant performance on long-term NaCl stress. In fact, no measure of K+ status was found to correlate with plant performance among cultivars either in the presence or absence of NaCl stress. By contrast, shoot Na+ accumulation showed the strongest correlation (a negative one) with biomass, under long-term salinity. Pharmacological evidence suggests that NaCl-induced K+ efflux is a result of membrane disintegrity, possibly as result of osmotic shock, and not due to ion-channel mediation. Taken together, we conclude that, in rice, K+ status (including efflux) is a poor predictor of salt tolerance and overall plant performance and, instead, shoot Na+ accumulation is the key factor in performance decline on NaCl stress.

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.…”

“…Cytsolic concentrations of K + and Na + ([K + ] cyt and [Na + ] cyt , respectively) and resting membrane potentials can alter with long-term Na + stress (Hajibagheri et al 1988;Flowers and Hajibagheri 2001;Carden et al 2003;Kronzucker et al 2006). b Sudden salinity stress can result in membrane disintegrity (osmotic shock) and the release of cellular contents, including K + and water (Nassery 1975;Cramer et al 1985;Britto et al 2010;Coskun et al 2013) K + provision (but not complete deprivation; Evans and Sorger 1966), or when K + uptake is partially inhibited, including by Na + itself (see above, and Figs. 1 and 2), Na + may well "rise to the challenge" of filling in for K + in more than one of its key functions.…”

“…Manifold as the effects of Na + on critical processes such as photosynthesis, transpiration, production of reactive oxygen species and, ultimately, growth and yield, are (Bazihizina et al 2012;Cheeseman 2013), many, if not most, of these must be considered as downstream effects rather than primary causes of toxicity. There is no doubt that Na + , when appearing suddenly at high concentrations, in "shock" scenarios (see discussion in Cheeseman 2013), carries osmotic consequences that disrupt, typically temporarily, the membrane integrity of roots (Britto et al 2010;Coskun et al 2013), or also those of shoots, such as shown in rice (Flowers et al 1991), preceding, or perhaps coinciding with, more "ion-specific" effects (see later discussions). In addition to this well-recognized osmotic effect, a second parsimonious explanation may lie in the disruption of potassium homeostasis-one that may reasonably and fruitfully supplant alternative, to date ill-substantiated , hypotheses, such as those of "toxic" Na + fluxes or cytosolic K + /Na + ratios (Maathuis and Amtmann 1999;Davenport and Tester 2000;Yao et al 2010; see below).…”

“…1a). Upon sudden, "shock", applications of higher concentrations of Na + , membrane disintegrity due to osmotic shock and ionic displacement (particularly of Ca 2+ ), result in the release of cellular contents, including K + and water (Nassery 1975(Nassery , 1979Lynch and Läuchli 1984;Cramer et al 1985;Britto et al 2010;Coskun et al 2013; Fig. 1b), offering an alternative, or additional, explanation of enhanced K + release under Na + exposure (Britto et al 2010;Coskun et al 2013).…”

“…Upon sudden, "shock", applications of higher concentrations of Na + , membrane disintegrity due to osmotic shock and ionic displacement (particularly of Ca 2+ ), result in the release of cellular contents, including K + and water (Nassery 1975(Nassery , 1979Lynch and Läuchli 1984;Cramer et al 1985;Britto et al 2010;Coskun et al 2013; Fig. 1b), offering an alternative, or additional, explanation of enhanced K + release under Na + exposure (Britto et al 2010;Coskun et al 2013). Combined, the above effects of impaired K + influx and enhanced efflux are expected to result in blockage of K + translocation to the shoot (Erdei and Kuiper 1979;Botella et al 1997;Kronzucker et al 2006;Munns and Tester 2008), with obvious consequences for downstream events such as photosynthesis and stomatal function.…”