High Affinity K⁺ Uptake in Maize Roots

Abstract

We report here on the putative coupling between a high affinity K+ uptake system which operates at low external K+ concentrations (Km = 10-20 micromolar), and H+ efflux in roots of intact, low-salt-grown maize plants. An experimental approach combining electrophysiological measurements, quantification of unidirectional K+("Rb+) influx, and the simultaneous measurement of net K+ and H+ fluxes associated with individual cells at the root surface with K@-and HW-selective microelectrodes was utilized.A microelectrode system described previously (IA Newman, LV Kochian, MA Grusak, and WJ Lucas [1987] Plant Physiol 84: 1177-1184) was used to quantify net ion fluxes from the measurement of electrochemical potential gradients for K+ and H+ ions within the unstirred layer at the root surface. No evidence for coupling between K+ uptake and H efflux could be found based on: (a) extremely variable K+:H+ flux stoichiometries, with K+ uptake often well in excess of H+ efflux; (b) dramatic timedependent variability in H+ extrusion when both fluxes were measured at a particular location along the root over time; and (c) a lack of pH sensitivity by the high affinity K uptake system (to changes in external pH) when net K+ uptake, unidirectional K ("Rb+) influx, and K+-induced depolarizations of the membrane potential were determined in uptake solutions buffered at pH values from pH 4 to 8. Based on the results presented here, we propose that high affinity active K+ absorption into maize root cells is not mediated by a K+/H+ exchange mechanism. Instead, it is either due to the operation of a K -H cotransport system, as has been hypothesized for Neurospora, or based on the striking lack of sensitivity to changes in extracellular pH, uptake could be mediated by a K+-ATPase as reported for Escherichia cofi and Saccharomyces.Although the mechanism(s) of K+ absorption into plant cells has not been elucidated, there is a persistent view in the literature that plasmalemma K+ influx is coupled to the active extrusion of protons (21,29 23,24,[26][27][28]. It should be noted here that interpretation of the literature in this area is complicated by the observation that different researchers have conducted their studies at different K+ concentrations, ranging from relatively low to quite high external concentrations (2 gM to 25 mM K+). Over this concentration range, it has been proposed that more than one K+ transport system may operate, and a general pattern emerges from the literature of a high affinity system at low external K+ levels, that is involved in active K+ absorption, operating in parallel with a low affinity system dominating uptake at high external K+ levels, which facilitates passive K+ uptake and quite likely involves K+ channels (4,5,8,15,18). Certainly any analysis of the mechanistic coupling of K+ influx to H+ extrusion must take into consideration the operation of multiple K+ transport systems, for the nature and degree of coupling to H+ efflux would certainly depend on the K+ transport system being investigated.Th...

Organic acids enhance the uptake of lead by wheat roots

“…Negatively charged plant root surface promote the development of an adjacent unstirred layer, and hence relatively high Pb 2+ concentration gradient near the roots. According to Kochian et al (1989), diffusive gradients in the unstirred layer around the roots or in the apoplast can occur and influence the uptake rate of elements, even in well-stirred solutions. Our results suggest that the unstirred layer was effectively thinner in the presence of organic acids, thus allowing Pb 2+ to be more readily absorbed or taken up by roots.…”

Role of the Plasma Membrane H+-ATPase in K+ Transport

“…Because the properties of H+ efflux were often observed to correlate with those of K+ influx when measured using bulk solution techniques (Poole, 1974;Behl and Raschke, 1987), it was argued that the plasma membrane H+-ATPase might be responsible for mediating active K+ uptake in coupled H + / K + exchange (for a discussion, see Kochian et al, 1989). However, a more detailed analysis of K+ and H+ fluxes measured using K+-and pH-sensitive microelectrodes by Kochian et al (1989) clearly demonstrated a lack of correlation between H+ efflux and K+ influx.…”

Can K+ Channels Do It All?

“…The pioneering tracer flux studies for root K+ uptake conducted by Epstein and coworkers (Epstein et al, 1963) indicated that at least two K+ transport mechanisms exist, one mediating high-affinity K+ uptake and the other low-affinity uptake. More recent studies in higher plants, fungi, and charophytic algae have shown that the high-affinity K+ transport system is expressed under growth in low K+ conditions, has a very low K, for K+ (2 to 20 pM), and is highly electrogenic (depolarizing) in nature (Rodriguez-Navarro et al, 1986;Kochian et al, 1989;Smith and Walker, 1989). K+ uptake into plants and fungi from low external K+ concentrations has generally been considered to involve a thermodynamically active process.…”

“…Consider K+ absorption into low saltgrown maize roots, for which we have previously characterized high-affinity K+ uptake (Kochian and Lucas, 1982;Newman et al, 1987;Kochian et al, 1989). The steady state net K+ influx into the maize root, measured using avibrating extracellular K+ microelectrode, was approximately 7 pmol cm-2 s l , and the E , measured simultaneously on the same root epidermal cell had a value of -110 mV.…”