K+ and pH homeostasis in plant cells is controlled by a synchronized K+ /H+ antiport at the plasma and vacuolar membrane

Abstract

Stomatal movement involves ion transport across the plasma membrane (PM) and vacuolar membrane (VM) of guard cells. However, the coupling mechanisms of ion transporters in both membranes and their interplay with Ca²⁺ and pH changes are largely unclear. Here, we investigated transporter networks in tobacco guard cells and mesophyll cells using multiparametric live-cell ion imaging and computational simulations. K⁺ and anion fluxes at both, PM and VM, affected H⁺ and Ca²⁺ , as changes in extracellular KCl or KNO₃ concentrations were accompanied by cytosolic and vacuolar pH shifts and changes in [Ca²⁺ ]_cyt and the membrane potential. At both membranes, the K⁺ transporter networks mediated an antiport of K⁺ and H⁺ . By contrast, net transport of anions was accompanied by parallel H⁺ transport, with differences in transport capacity for chloride and nitrate. Guard and mesophyll cells exhibited similarities in K⁺ /H⁺ transport but cell type-specific differences in [H⁺ ]_cyt and pH-dependent [Ca²⁺ ]_cyt signals. Computational cell biology models explained mechanistically the properties of transporter networks and the coupling of transport across the PM and VM. Our integrated approach indicates fundamental principles of coupled ion transport at membrane sandwiches to control H⁺ /K⁺ homeostasis and points to transceptor-like Ca²⁺ /H⁺ -based ion signaling in plant cells.

Keywords: calcium; guard cells; homeostasis; mathematical modeling; pH; potassium; stomata; transporters.