A mechanism for sensing of and adaptation to K+ deprivation in plants

Abstract

Potassium ions (K+) are essential for manifold cellular processes. Organismal K+ homoeostasis requires sensing of K+ availability, efficient uptake and defined distribution. Roots are the organ for K+ uptake in plants and soil K+ availability shapes root growth and architecture1. Important channels and transporters conveying cellular K+ fluxes have been described2,3. Understanding K+ sensing and the mechanisms that orchestrate downstream responses exemplifies how environmental conditions integrate with root development and is essential to advance plant nutrition for sustainable agriculture. Here, we report where plants sense K+ deprivation and how this translates into spatially defined ROS signals to trigger HAK5 K+ uptake transporter induction and accelerated maturation of the Casparian strip (CS) paracellular barrier. We define the organ scale K+ pattern of roots and identify a postmeristematic K+-sensing niche (KSN) defined by rapid K+ decline and Ca2+ signals. We discover a Ca2+-triggered bifurcating low-K+ signalling (LKS) axis in that LK-enhanced CIF peptide signalling reinforces SGN3-LKS4/SGN1 receptor kinase complex activation. As consequence, activation of the NOXs RBOHC and RBOHD conveys transcriptome adaptation including HAK5 induction and accelerated CS maturation superimposed on the RBOHF-executed default CS formation. These mechanisms synchronise developmental differentiation and transcriptome reprogramming for maintaining K+ homoeostasis and optimising nutrient foraging by roots.