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. This study reveals ABA-triggered low-nanomolar Ca2+ dynamics in diverse plant organs and cell types using an ultrasensitive Ca2+ biosensor. Spatiotemporal Ca2+ dynamics modulate the root cap cycle in adaptation to stress through ABA–Ca2+–CPK signalling.