Plasma-membrane electrical responses to salt and osmotic gradients contradict radiotracer kinetics, and reveal Na+-transport dynamics in rice (Oryza sativa L.)

Hamam, Ahmed M.; Coskun, Devrim; Britto, Dev T.; Plett, Darren; Kronzucker, Herbert J.

doi:10.1007/s00425-018-3059-7

Plasma-membrane electrical responses to salt and osmotic gradients contradict radiotracer kinetics, and reveal Na⁺-transport dynamics in rice (Oryza sativa L.)

Original Article
Published: 29 November 2018

Volume 249, pages 1037–1051, (2019)
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Ahmed M. Hamam¹,
Devrim Coskun²,
Dev T. Britto¹,
Darren Plett³ &
…
Herbert J. Kronzucker³

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Abstract

Main conclusion

A systematic analysis of NaCl-dependent, plasma-membrane depolarization (∆∆Ψ) in rice roots calls into question the current leading model of rapid membrane cycling of Na⁺ under salt stress.

To investigate the character and mechanisms of Na⁺ influx into roots, Na⁺-dependent changes in plasma-membrane electrical potentials (∆∆Ψ) were measured in root cells of intact rice (Oryza sativa L., cv. Pokkali) seedlings. As external sodium concentrations ([Na⁺]_ext) were increased in a step gradient from 0 to 100 mM, membrane potentials depolarized in a saturable manner, fitting a Michaelis–Menten model and contradicting the linear (non-saturating) models developed from radiotracer studies. Clear differences in saturation patterns were found between plants grown under low- and high-nutrient (LN and HN) conditions, with LN plants showing greater depolarization and higher affinity for Na⁺ (i.e., higher V_max and lower K_m) than HN plants. In addition, counterion effects on ∆∆Ψ were pronounced in LN plants (with ∆∆Ψ decreasing in the order: Cl⁻ > SO₄²⁻ > HPO ^2-₄ ), but not seen in HN plants. When effects of osmotic strength, Cl⁻ influx, K⁺ efflux, and H⁺-ATPase activity on ∆∆Ψ were accounted for, resultant K_m and V_max values suggested that a single, dominant Na⁺-transport mechanism was operating under each nutritional condition, with K_m values of 1.2 and 16 mM for LN and HN plants, respectively. Comparing saturating patterns of depolarization to linear patterns of ²⁴Na⁺ radiotracer influx leads to the conclusion that electrophysiological and tracer methods do not report the same phenomena and that the current model of rapid transmembrane sodium cycling may require revision.

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Potassium and Sodium Transport Channels Under NaCl Stress

Salt-induced NO3 - uptake inhibition in cowpea roots is dependent on the ionic composition of the salt and its osmotic effect

Article 13 April 2016

Na+ Sensing, Transport, and Plant Salt Tolerance

Abbreviations

∆∆Ψ:: Change in plasma-membrane electrical potential
HN:: High nutrient
LN:: Low nutrient
NMDG-Cl:: N-Methyl-d-glucamine chloride
NSCC:: Non-selective cation channel
RTSC:: Rapid transmembrane sodium cycling

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Acknowledgements

We thank M. Butler and R. Pasuta at McMaster Nuclear Reactor (Hamilton, Ontario, Canada) for supplying ²⁴Na⁺ and ⁴²K⁺. We also thank Dr. D. Dubins at the University of Toronto Leslie Dan Faculty of Pharmacy for access to their osmometer. This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC), the Ontario Graduate Student Scholarship (OGS), and the University of Toronto.

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Department of Biological Sciences and Canadian Centre for World Hunger Research (CCWHR), University of Toronto, Toronto, ON, M1C 1A4, Canada
Ahmed M. Hamam & Dev T. Britto
Département de Phytologie, Faculté des Sciences de l’Agriculture et de l’Alimentation (FSAA), Université Laval, Québec, QC, G1V 0A6, Canada
Devrim Coskun
School of Agriculture and Food, Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Melbourne, VIC, 3010, Australia
Darren Plett & Herbert J. Kronzucker

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Ahmed M. Hamam
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Dev T. Britto
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Suppl. Fig. S1

Sodium-dependent membrane depolarization (∆Ψ) in root cortical and epidermal cells of intact rice seedings, cv. Pokkali. Plants were grown as in Fig. 1 under HN conditions, then subjected to stepwise increases in external concentration of NaCl. With each increase in NaCl concentration, the ∆ψ was allowed to saturate before the next stepwise increase in concentration was washed in (TIFF 307 kb)

Suppl. Fig. S2 a

Sodium-dependent membrane depolarization (∆∆Ψ) in root cortical and epidermal cells of intact rice seedlings, cv. IR29. Plants were grown as in Fig. 1, then subjected to stepwise increases in external concentration of NaCl; error bars generated via error propagation. Error bars represent ± SE. b Sodium-dependent membrane depolarization (∆ψ) in root cortical and epidermal cells of intact rice seedings, cv. IR29. Plants were grown as in Fig. 1 under HN conditions, then subjected to a stepwise increases in external concentration of NaCl. With each increase in NaCl concentration, the ∆ψ was allowed to saturate before the next stepwise increase in concentration was washed in (TIFF 1076 kb)

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Hamam, A.M., Coskun, D., Britto, D.T. et al. Plasma-membrane electrical responses to salt and osmotic gradients contradict radiotracer kinetics, and reveal Na⁺-transport dynamics in rice (Oryza sativa L.). Planta 249, 1037–1051 (2019). https://doi.org/10.1007/s00425-018-3059-7

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