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

Potassium (K+) acquisition in roots is generally 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 (>1 mM) [K+]ext. Radiotracer measurements in the LATS range indicate that the linear rise in influx continues well beyond nutritionally relevant concentrations (>10 mM), suggesting K+ transport may be pushed to extraordinary, and seemingly limitless, capacity. Here, we assess this rise, asking whether LATS measurements faithfully report transmembrane fluxes. Using 42K+-isotope and electrophysiological methods in barley, we show that this flux is part of a K+-transport cycle through the apoplast, 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 PTS, an apoplastic tracer. A linear apoplastic influx, masking a saturating transmembrane influx, was also found in Arabidopsis mutants lacking the K+ transporters AtHAK5 and AtAKT1. Our work significantly revises the model of K+ transport by demonstrating a surprisingly modest upper limit for plasma-membrane influx, and offers insight into sodium transport under salt stress.