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, CO2 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.