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

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.

Keywords: Arabidopsis thaliana; K+ channel; calcium; cameleon YC3.6; high-resolution calcium imaging; nutrient starvation; potassium; signaling.