ABA-activated low-nanomolar Ca2+–CPK signalling controls root cap cycle plasticity and stress adaptation

Abstract

Abscisic acid (ABA) regulates plant stress adaptation, growth and reproduction. Despite extensive ABA–Ca²⁺ signalling links, imaging ABA-induced increases in Ca²⁺ concentration has been challenging, except in guard cells. Here we visualize ABA-triggered [Ca²⁺] dynamics in diverse organs and cell types of Arabidopsis thaliana using a genetically encoded Ca²⁺ ratiometric sensor with a low-nanomolar Ca²⁺-binding affinity and a large dynamic range. The subcellular-targeted Ca²⁺ ratiometric sensor reveals time-resolved and unique spatiotemporal Ca²⁺ signatures from the initial plasma-membrane nanodomain, to cytosol, to nuclear oscillation. Via receptors and sucrose-non-fermenting1-related protein kinases (SnRK2.2/2.3/2.6), ABA activates low-nanomolar Ca²⁺ transient and Ca²⁺-sensor protein kinase (CPK10/30/32) signalling in the root cap cycle from stem cells to cell detachment. Surprisingly, unlike the prevailing NaCl-stimulated micromolar Ca²⁺ spike, salt stress induces a low-nanomolar Ca²⁺ transient through ABA signalling, repressing key transcription factors that dictate cell fate and enzymes that are crucial to root cap maturation and slough. Our findings uncover ABA–Ca²⁺–CPK signalling that modulates root cap cycle plasticity in adaptation to adverse environments.