Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants

Significance This work documents a previously unreported plant-wide signaling system based on the rapid, long-distance transmission of Ca2+ waves. In the root these waves move through the cortical and endodermal cell layers at speeds of up to 400 µm/s, i.e., traversing several cells per second. This Ca2+ wave system correlates with the triggering of molecular responses in distant parts of the plant upon perception of localized (salt) stress. Such propagating Ca2+ waves provide a new mechanism for the rapid integration of activities throughout the plant body. Their sessile lifestyle means that plants have to be exquisitely sensitive to their environment, integrating many signals to appropriate developmental and physiological responses. Stimuli ranging from wounding and pathogen attack to the distribution of water and nutrients in the soil are frequently presented in a localized manner but responses are often elicited throughout the plant. Such systemic signaling is thought to operate through the redistribution of a host of chemical regulators including peptides, RNAs, ions, metabolites, and hormones. However, there are hints of a much more rapid communication network that has been proposed to involve signals ranging from action and system potentials to reactive oxygen species. We now show that plants also possess a rapid stress signaling system based on Ca2+ waves that propagate through the plant at rates of up to ∼400 µm/s. In the case of local salt stress to the Arabidopsis thaliana root, Ca2+ wave propagation is channeled through the cortex and endodermal cell layers and this movement is dependent on the vacuolar ion channel TPC1. We also provide evidence that the Ca2+ wave/TPC1 system likely elicits systemic molecular responses in target organs and may contribute to whole-plant stress tolerance. These results suggest that, although plants do not have a nervous system, they do possess a sensory network that uses ion fluxes moving through defined cell types to rapidly transmit information between distant sites within the organism.