Rapid, futile K+ cycling and pool-size dynamics define low-affinity potassium transport in barley.
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 > or = 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.
Szczerba
Mark W
MW
Department of Life Sciences, University of Toronto, Toronto, Ontario, Canada M1C 1A4.
Britto
Dev T
DT
Kronzucker
Herbert J
HJ
D001692:Biological Transport; D002462:Cell Membrane / Q000378:metabolism; D003600:Cytosol / Q000378:metabolism; D006706:Homeostasis / Q000187:drug effects; D001467:Hordeum / Q000166:cytology / Q000187:drug effects / Q000378:metabolism*; D007700:Kinetics; D008564:Membrane Potentials; D009584:Nitrogen / Q000494:pharmacology; D018517:Plant Roots / Q000166:cytology / Q000187:drug effects / Q000378:metabolism; D018520:Plant Shoots / Q000166:cytology / Q000187:drug effects / Q000378:metabolism; D011188:Potassium / Q000378:metabolism* / Q000494:pharmacology; D036226:Seedlings / Q000378:metabolism
D009584:Nitrogen; D011188:Potassium