Significance People for centuries are puzzled how living creatures like plants sense their environment. Plants employ electrical signals to communicate a cue-dependent local status between plants cells and organs. As a first response to biotic and abiotic stresses, the membrane potential of plant cells depolarizes. Recovery from the depolarized state, repolarization, was proposed to involve ion channels and pumps. Here, we established channelrhodopsin (ChR2)-based optogenetics in plants and learned that the plant plasma membrane H ⁺ -ATPase represents the major driver of membrane potential repolarization control during plant electrical signaling, rather than voltage-dependent ion channels.