K+ efflux and retention in response to NaCl stress do not predict salt tolerance in contrasting genotypes of rice (Oryza sativa L.).

Devrim Coskun,Inci Tolay,Herbert J Kronzucker,Imtiaz Kabir,Yuel-Kai Jean,Ayfer A Torun,Dev T Britto

doi:10.1371/journal.pone.0057767

Devrim Coskun, Inci Tolay + Show 5 more

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https://doi.org/10.1371/journal.pone.0057767

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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.

Highlights

Soil salinity, predominantly in the form of NaCl, is a major agricultural issue, in irrigated areas [1,2], where as much as one third of the world’s food production takes place and nearly half of the land is afflicted ([3] and references therein)
Potassium is critical to the proper functioning of plant cells for reasons that include charge balancing in the cytoplasm, enzyme activation, and the maintenance of cell turgor [8,9]
No measure of K+ fluxes or accumulation could predict plant performance in the presence or absence of NaCl stress, and that instead, shoot Na+ content was the best indicator of performance on high salinity, albeit after the fact

Summary

Introduction

Predominantly in the form of NaCl, is a major agricultural issue, in irrigated areas [1,2], where as much as one third of the world’s food production takes place and nearly half of the land is afflicted ([3] and references therein). An alternative explanation is that high amounts of NaCl compromises the integrity of the plasma membrane, due to ionic and osmotic effects, resulting in release of cellular contents, including K+ [12,15,16] Understanding this phenomenon would provide important insight into uncovering the elusive nature of salt toxicity [5,17], and would allow for critical assessment of the relevance of stimulated K+ efflux to other aspects of salt stress, such as the inhibition of primary K+ uptake, cytosolic K+:Na+ ratios, primary Na+ uptake, and shoot Na+ accumulation [4,5,12,18,19]

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