How high do ion fluxes go? A re-evaluation of the two-mechanism model of K+ 2 transport in plant roots

Authors: COSKUN, DEVRIM - University Of Toronto; BRITTO, DEV - University Of Toronto; Kochian, Leon; KRONZUCKER, HERBERT - University Of Toronto

Submitted to: Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/8/2015
Publication Date: 12/11/2015
Citation: Coskun, D., Britto, D.T., Kochian, L.V., Kronzucker, H.J. 2015. How high do ion fluxes go? A re-evaluation of the two-mechanism model of K+ 2 transport in plant roots. Plant Science. 243:96-104.

Interpretive Summary: Potassium (K) is one of the most important plant mineral nutrients and is the most abundant cellular cation in plant cells. Hence, plant root K uptake has been one of the most widely studied plant processes, with hundreds of publications on the physiology, membrane biophysics, genetics and molecular biology of root K uptake and plant K transport. It is widely accepted, based on detailed analyses of the concentration-dependent kinetics of root K uptake, that K uptake into roots is mediated by two independent processes. At low soil K concentrations, a high affinity and thermodynamically active uptake system has been proposed, mediating K uptake against its thermodynamic gradient. This system follows conventional saturating concentration-dependent kinetics. At higher soil K concentrations, a low affinity K uptake system following linear concentration dependent kinetics that does not saturate is believed to operate, and is mediated by root plasma membrane K channels that allows K ions to flow into the root cell down their thermodynamic gradient. The work presented in this paper is the result of a careful physiological and thermodynamic analysis of root K uptake in barley and Arabidopsis. The findings clearly show that the low affinity, linear K uptake system is not actually K transport into root cells at all. Instead it is an artifact due to K isotope cycling within the root cell wall (apoplast), which was missed by earlier methods that did not properly remove the cell wall K isotope cation that was bound to fixed negative charges in the cell wall. These findings are important, as they call for a fundamental revision of mineral ion flux models in plant roots, and will apply to low-affinity fluxes of other ions, particularly those of Na+ which has been widely investigated due to the growing problem of salinity stress on agricultural soils.

Technical Abstract: Potassium acquisition in roots is described by a two-mechanism model, consisting of a saturable, high-affinity transport system (HATS) operating via H+/K+ symport at low (< 1 mM) external [K+] ([K+]ext), and a linear, low-affinity system (LATS) operating via ion channels at high (> 112 mM) [K+]ext. Radiotracer measurements in the LATS range indicate that the linear rise in K+ influx continues well beyond nutritionally relevant concentrations (> 10 mM), suggesting that K+ transport has unlimited capacity. Here, we assess this linear rise, asking whether LATS measurements faithfully report transmembrane fluxes. Using 42K+-isotope, pharmacological, and electrophysiological methods in barley, we show that this linear flux is part of a K+-transport cycle through the extracellular (apoplastic) matrix, and masks a genuine plasma-membrane influx that displays Michaelis-Menten kinetics. Rapid apoplastic cycling of K+ is corroborated by an absence of transmembrane 42K+ efflux above 1 mM, and by the efflux kinetics of 8-hydroxy-1,3,6-pyrenetrisulphonic acid, an apoplastic tracer. A linear apoplastic K+ influx, masking a saturating transmembrane influx, was also found in Arabidopsis mutants lacking the K+ transporters AtHAK5 and AtAKT1. Our work revises K+-transport models by demonstrating a surprisingly modest upper limit for plasma-membrane influx, and offers insight into Na+ transport under salt stress.