Plant cells maintain high Ca(2+) concentration gradients between the cytosol and the extracellular matrix, as well as intracellular compartments. During evolution, the regulatory mechanisms, maintaining low cytosolic free Ca(2+) concentrations, most likely provided the backbone for the development of Ca(2+)-dependent signalling pathways. In this review, the current understanding of molecular mechanisms involved in Ca(2+) homeostasis of plants cells is evaluated. The question is addressed to which extent the mechanisms, controlling the cytosolic Ca(2+) concentration, are linked to Ca(2+)-based signalling. A large number of environmental stimuli can evoke Ca(2+) signals, but the Ca(2+)-induced responses are likely to differ depending on the stimulus applied. Two mechanisms are put forward to explain signal specificity of Ca(2+)-dependent responses. A signal may evoke a specific Ca(2+) signature that is recognized by downstream signalling components. Alternatively, Ca(2+) signals are accompanied by Ca(2+)-independent signalling events that determine the specificity of the response. The existence of such parallel-acting pathways explains why guard cell responses to abscisic acid (ABA) can occur in the absence, as well as in the presence, of Ca(2+) signals. Future research may shed new light on the relation between parallel acting Ca(2+)-dependent and -independent events, and may provide insights in their evolutionary origin.