At least four genes encoding plasma membrane inward K ⁺ channels (K _in channels) are expressed in Arabidopsis guard cells. A double mutant plant was engineered by disruption of a major K _in channel gene and expression of a dominant negative channel construct. Using the patch-clamp technique revealed that this mutant was totally deprived of guard cell K _in channel (GCK _in ) activity, providing a model to investigate the roles of this activity in the plant. GCK _in activity was found to be an essential effector of stomatal opening triggered by membrane hyperpolarization and thereby of blue light-induced stomatal opening at dawn. It improved stomatal reactivity to external or internal signals (light, CO ₂ availability, and evaporative demand). It protected stomatal function against detrimental effects of Na ⁺ when plants were grown in the presence of physiological concentrations of this cation, probably by enabling guard cells to selectively and rapidly take up K ⁺ instead of Na ⁺ during stomatal opening, thereby preventing deleterious effects of Na ⁺ on stomatal closure. It was also shown to be a key component of the mechanisms that underlie the circadian rhythm of stomatal opening, which is known to gate stomatal responses to extracellular and intracellular signals. Finally, in a meteorological scenario with higher light intensity during the first hours of the photophase, GCK _in activity was found to allow a strong increase (35%) in plant biomass production. Thus, a large diversity of approaches indicates that GCK _in activity plays pleiotropic roles that crucially contribute to plant adaptation to fluctuating and stressing natural environments.