High salinity tolerance in the stl2 mutation of Ceratopteris richardii is associated with enhanced K⁺ influx and loss

Abstract

The roles of K+ uptake and loss in the salinity response of the wild type and the salt‐tolerant mutant stl2 of Ceratopteris richardii were studied by measuring Rb+ influx and loss and the effects of Na+, Mg2+, Ca2+ and K+‐transport inhibitors. In addition, electrophysiological responses were measured for both K+ and Rb+ and for the effects of Na+ and NH4+ on subsequent K+‐induced depolarizations. stl2 had a 26–40% higher uptake rate for Rb+ than the wild type at 0.5–10 mol m−3 RbCl. Similarly, membrane depolarizations induced by both RbCl and KCl were consistently greater in stl2. In the presence of 0–180 mol m−3 NaCl, stl2 maintained a consistently greater Rb+ influx than the wild type. stl2 retained a greater capacity for subsequent KCl‐induced depolarization following exposure to NaCl. Five mol m−3 Mg2+ decreased Rb+ uptake in stl2; however, additional Mg2+ up to 40 mol m−3 did not affect Rb+ uptake further. Ca2+ supplementation resulted in a very minor decrease of Rb+ uptake that was similar in the two genotypes. Tetraethylammonium chloride and CsCl gave similar inhibition of Rb+ uptake in both genotypes, but NH4Cl gave substantially greater inhibition in the wild type than in stl2. NH4Cl resulted in a greater membrane depolarization in the wild type and the capacity for subsequent depolarization by KCl was markedly reduced. stl2 exhibited a higher Independent loss of Rb+ than the wild type, but, in the absence of external K+, loss of Rb+ was equivalent in the two genotypes. Since constitutive K+ contents are nearly identical, we conclude that high K+ influx and loss exact a metabolic cost that is reflected in the inhibition of gametophytic growth. Growth inhibition can be alleviated by reduced supplemental K+ or by treatments that slightly reduce K+ influx, such as moderate concentrations of Na+ or Mg2+. We propose that high throughput of K+ allows maintenance of cytosolic K+ under salt stress and that a high uptake rate for K+ results in a reduced capacity for the entrance and accumulation of alternative cations such as Na+ in the cytosol.

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

“…Much of this salinization is attributable to the infiltration and accumulation of NaCl (Zhu, 2001; Munns, 2005), often resulting in soil Na + concentrations above 40 mM, and growth suppression in most crops (Munns, 2005). One of the key physiological processes disrupted by Na + supply in this toxic range is the maintenance of cellular and whole-plant potassium homeostasis (Rains and Epstein, 1967; Flowers and Läuchli, 1983; Watad et al , 1991; Gaxiola et al , 1992; Warne et al , 1996; Zhu et al , 1998; Santa-María and Epstein, 2001; Peng et al , 2004; Cakmak, 2005; Kader and Lindberg, 2005; Kronzucker et al , 2006; Takahashi et al , 2007). At the tissue level, the ratio of K + to Na + is considered an excellent indicator of plant tolerance to salinity; the higher the ratio, the higher the plant's tolerance (Flowers and Hajibagheri, 2001; Cakmak, 2005; Chen et al , 2007 b ; cf.…”

Sodium as nutrient and toxicant

“…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).…”

The cytosolic Na+ : K+ ratio does not explain salinity‐induced growth impairment in barley: a dual‐tracer study using 42K+ and 24Na+

“…In such soils, NaCl concentrations typically exceed 40 mM, and much higher values are frequently found (Munns 2005), creating toxic growth conditions for most plants, including all major crop species. It has long been known that NaCl toxicity is largely attributable to the effects of Na + , and only rarely those of Cl − , and that Na + toxicity is linked strongly to the plant's ability to sustain the acquisition and in planta distribution of K + (Rains & Epstein 1967;Warne et al . 1996;Zhu, Liu & Xiong 1998;Tyerman & Skerrett 1999;Kader & Lindberg 2005).…”