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Published on June 30, 2006; 10.1104/pp.106.082701


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Received April 27, 2006
Accepted June 17, 2006

Rapid, futile K+ cycling and pool-size dynamics define low-affinity potassium transport in barley

Mark W. Szczerba , Dev T. Britto , and Herbert J. Kronzucker *

Department of Life Sciences, University of Toronto, 1265 Military Trail, Toronto, Ontario, Canada, M1C 1A4

* Corresponding author; email: herbertk{at}utsc.utoronto.ca.

Using the short-lived radiotracer 42K+, we present the first comprehensive subcellular flux analysis of low-affinity K+ transport in plants. We overturn the paradigm of cytosolic K+ pool-size ([K+]cyt) 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 2-3 times lower than are characteristic of high-affinity transport (HATS). 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 (HATS or LATS), 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 [K+]cyt, 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.




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