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WHOLE PLANT AND ECOPHYSIOLOGY

Rapid, Futile K⁺ Cycling and Pool-Size Dynamics Define Low-Affinity Potassium Transport in Barley¹

Department of Life Sciences, University of Toronto, Toronto, Ontario, Canada M1C 1A4

Using the short-lived radiotracer ⁴²K⁺, we present a comprehensive subcellular flux analysis of low-affinity K⁺ transport in plants. We overturn the paradigm of cytosolic K⁺ pool-size homeostasis and demonstrate that low-affinity K⁺ transport is characterized by futile cycling of K⁺ at the plasma membrane. Using two methods of compartmental analysis in intact seedlings of barley (Hordeum vulgare L. cv Klondike), we present data for steady-state unidirectional influx, efflux, net flux, cytosolic pool size, and exchange kinetics, and show that, with increasing external [K⁺] ([K⁺]_ext), both influx and efflux increase dramatically, and that the ratio of efflux to influx exceeds 70% at [K⁺]_ext 20 mM. Increasing [K⁺]_ext, furthermore, leads to a shortening of the half-time for cytosolic K⁺ exchange, to values 2 to 3 times lower than are characteristic of high-affinity transport. Cytosolic K⁺ concentrations are shown to vary between 40 and 200 mM, depending on [K⁺]_ext, on nitrogen treatment (NO₃^– or NH₄⁺), and on the dominant mode of transport (high- or low-affinity transport), illustrating the dynamic nature of the cytosolic K⁺ pool, rather than its homeostatic maintenance. Based on measurements of trans-plasma membrane electrical potential, estimates of cytosolic K⁺ pool size, and the magnitude of unidirectional K⁺ fluxes, we describe efflux as the most energetically demanding of the cellular K⁺ fluxes that constitute low-affinity transport.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Herbert J. Kronzucker (herbertk{at}utsc.utoronto.ca).

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.106.082701.

^* Corresponding author; e-mail herbertk{at}utsc.utoronto.ca; fax 416–287–7642.

Received April 27, 2006; returned for revision June 1, 2006; accepted June 17, 2006.

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