Two types of anion channel currents in guard cells with distinct voltage regulation

Abstract

Transpirational water loss by plants is reduced by closing of stomatal pores in the leaf epidermis. Anion channels in the plasma membrane of guard cells may provide a key molecular mechanism for control of stomatal closing in leaves. However, central questions regarding the regulation, diversity, and function of anion channels in guard cells and other higher plant cells remain unanswered. We show here that two highly distinct types of depolarization-activated anion currents operate in the plasma membrane of Vicia faba guard cells. One described type of anion channel was activated rapidly within 50 ms by depolarization, inactivated during prolonged stimulation, and deactivated rapidly at hyperpolarized potentials (R-type anion current). The other depolarization-activated anion current showed extremely slow voltage-dependent activation and deactivation (S-type anion current) and lacked inactivation. The distinct voltage and time dependencies of R-type and S-type anion channels suggest that they may play a role during depolarization-associated signal transduction in higher plant cells and that these anion channels may contribute to different processes in the regulation of stomatal movements. In particular, the slow and sustained nature of S-type anion channel activation revealed here leads us to hypothesize that S-type anion channels may provide a central molecular mechanism for control of stomatal closing, which is accompanied by long-term anion efflux and depolarization.