Two spatially and temporally distinct Ca2+ signals convey Arabidopsis thaliana responses to K+ deficiency

Behera S., Long Y., Schmitz-Thom I., Wang X., Zhang C., Li H., Steinhorst L., Manishankar P., Ren X., Offenborn J., Wu W., Kudla J., Wang Y.

Abstract

In plants, potassium (K+) homeostasis is tightly regulated and established against a concentration gradient to the environment. Despite the identification of Ca2+-regulated kinases as modulators of K+ channels, the immediate signaling and adaptation mechanisms of plants to low-K+ conditions are only partially understood. To assess the occurrence and role of Ca2+ signals in Arabidopsis thaliana roots, we employed ratiometric analyses of Ca2+ dynamics in plants expressing the Ca2+ reporter YC3.6 in combination with patch-clamp analyses of root cells and two-electrode voltage clamp (TEVC) analyses in Xenopus laevis oocytes. K+ deficiency triggers two successive and distinct Ca2+ signals in roots exhibiting spatial and temporal specificity. A transient primary Ca2+ signature arose within 1 min in the postmeristematic stelar tissue of the elongation zone, while a secondary Ca2+ response occurred after several hours as sustained Ca2+ elevation in defined tissues of the elongation and root hair differentiation zones. Patch-clamp and TEVC analyses revealed Ca2+ dependence of the activation of the K+ channel AKT1 by the CBL1–CIPK23 Ca2+ sensor-kinase complex. Together, these findings identify a critical role of cell group-specific Ca2+ signaling in low K+ responses and indicate an essential and direct role of Ca2+ signals for AKT1 K+ channel activation in roots.