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 (42)K(+) and (24)Na(+) 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.

Keywords: Barley; compartmental analysis; cytosol; efflux; influx; potassium; radiotracers; salinity; salt stress; sodium.

Fig. 1.

Representative plots of ⁴²K⁺ and ²⁴Na⁺ (inset) efflux from roots of intact barley seedlings, under varying ionic conditions. Roots had been preloaded for 60 min in radioactive solution, then eluted of radioactivity in a timed series of non-radioactive growth-solution aliquots. Dashed lines represent the slowest exchanging compartment (cytosolic), with a minimum of 12 time points used for linear regression. Experiments were replicated between 4 and 14 times.

Fig. 2.

Components of unidirectional K⁺ influx in roots of intact barley seedlings, grown and monitored with or without 100 mM Na⁺. Control values are drawn from Szczerba et al. (2006). Error bars refer to ±SEM of 4–14 replicates, with asterisks indicating significant differences in influx values within a given K⁺ treatment (P < 0.05). Where differences in influx between Na⁺ treatments were observed, significant differences in efflux and net flux were also found (P < 0.05).

Fig. 3.

Components of unidirectional Na⁺ influx in roots of intact barley seedlings, grown and monitored at 100 mM Na⁺ and at varying external K⁺ provision. Error bars refer to ±SEM of four to seven replicates. No significant differences between treatments were observed.

Fig. 4.

Tissue content of K⁺ in roots and shoots of barley plants, grown with or without 100 mM Na⁺, and under varying external K⁺ provision. Control (1 mM Na⁺) values are drawn from Szczerba et al. (2006). Error bars refer to ±SEM of four to eight replicates. Asterisks denote significant differences within a given K⁺ treatment and plant organ (P < 0.05).

Fig. 5.

Tissue content of Na⁺ in roots and shoots of barley plants, grown at 100 mM Na⁺, and under varying external K⁺ provision. Error bars refer to ±SEM of 8–12 replicates. No significant differences between treatments were observed.

Fig. 6.

Cytosolic K⁺ activity in roots of barley seedlings grown under varying K⁺ provision, with or without 100 mM Na⁺. Error bars refer to ±SEM of 4–14 replicates. Asterisks denote significant differences within a given K⁺ treatment (P < 0.05).

Fig. 7.

Cytosolic Na⁺ activity in roots of barley seedlings grown under 100 mM Na⁺ and varying K⁺ provision. Error bars refer to ±SEM of four to seven replicates. No significant differences between treatments were observed.

Fig. 8.

Cytosolic and tissue K⁺:Na⁺ ratios in roots of intact barley seedlings, grown at 100 mM Na⁺ and varying K⁺ provision.

Fig. 9.

(A) Fresh weights of barley seedlings (roots+shoots), grown and monitored with or without 100 mM Na⁺ and varying levels of K⁺ supply. Error bars refer to ±SEM of 12–72 replicates. Asterisks denote significant differences within a given K⁺ treatment (P < 0.05). (B) Fresh weights of barley seedlings (roots+shoots), grown and monitored with or without 100 mM Na⁺ and two different [K⁺]_ext (1.5 mM and 40 mM) for 2 weeks. Error bars refer to ±SEM of 5–82 replicates.