Arabidopsis HAK5 under low K⁺ availability operates as PMF powered high-affinity K⁺ transporter

Plants can survive in soils of low micromolar potassium (K⁺) concentrations. Root K⁺ intake is accomplished by the K⁺ channel AKT1 and KUP/HAK/KT type high-affinity K⁺ transporters. Arabidopsis HAK5 mutants impaired in low K⁺ acquisition have been identified already more than two decades ago, the molecular mechanism, however, is still a matter of debate also because of lack of direct measurements of HAK5-mediated K⁺ currents. When we expressed AtHAK5 in Xenopus oocytes together with CBL1/CIPK23, no inward currents were elicited in sufficient K⁺ media. Under low K⁺ and inward-directed proton motive force (PMF), the inward K⁺ current increased indicating that HAK5 energetically couples the uphill transport of K⁺ to the downhill flux of H⁺. At extracellular K⁺ concentrations above 25 μM, the initial rise in current was followed by a concentration-graded inactivation. When we replaced Tyr450 in AtHAK5 to Ala the K⁺ affinity strongly decreased, indicating that AtHAK5 position Y450 holds a key for K⁺ sensing and transport. When the soil K⁺ concentration drops toward the range that thermodynamically cannot be covered by AKT1, the AtHAK5 K⁺/H⁺ symporter progressively takes over K⁺ nutrition. Therefore, optimizing K⁺ use efficiency of crops, HAK5 could be key for low K⁺ tolerant agriculture.