Potassium is an inevitable component of plant life, and potassium channels play a pivotal role in plant growth and development. The role of potassium and of K(+) channels in plant cell division and cell-cycle progression, however, has not been determined so far. K(+) channel blocker studies with synchronized tobacco BY-2 cells revealed that K(+) uptake is required for proper cell-cycle progression during the transition from G(1) to S phase. Electrophysiological studies (patch-clamp and voltage-clamp techniques) showed a cell-cycle dependency of K(+) channel activities and reduced driving force for K(+) uptake in dividing cells. Among the four Shaker-like K(+) channel genes expressed in BY-2 cells, NKT1 represents an inwardly rectifying K(+) channel that mediates K(+) uptake. NKT1 is transcriptionally induced during G(1) phase, while transcripts of the outward-rectifier NTORK1 dominate S phase. Elongating BY-2 cells appeared hyperpolarized (-101 +/- 11 mV), and had elevated osmotic pressure and approximately twice the turgor pressure when compared with depolarized (-64 +/- 8 mV) dividing cells. This indicates that cells have to gain a threshold K(+) level to re-enter the cell cycle. Based on these findings, turgor regulation through modulation of K(+) channel density in plant cell division and cell-cycle progression is discussed.