A potassium-sensing niche in Arabidopsis roots orchestrates signaling and adaptation responses to maintain nutrient homeostasis

Wu W.H., Schmitz-Thom I., Wang Y., Kudla J., Wang F.L., Tan Y.L., Wallrad L., Du X.Q., Eickelkamp A., Wang Z.F., He G.F., Rehms F., Li Z., Han J.P.

Abstract

Organismal homeostasis of the essential ion K+ requires sensing of its availability, efficient uptake, and defined distribution. Understanding plant K+ nutrition is essential to advance sustainable agriculture, but the mechanisms underlying K+ sensing and the orchestration of downstream responses have remained largely elusive. Here, we report where plants sense K+ deprivation and how this translates into spatially defined ROS signals to govern specific downstream responses. We define the organ-scale K+ pattern of roots and identify a postmeristematic K+-sensing niche (KSN) where rapid K+ decline and Ca2+ signals coincide. Moreover, we outline a bifurcating low-K+-signaling axis of CIF peptide-activated SGN3-LKS4/SGN1 receptor complexes that convey low-K+-triggered phosphorylation of the NADPH oxidases RBOHC, RBOHD, and RBOHF. The resulting ROS signals simultaneously convey HAK5 K+ uptake-transporter induction and accelerated Casparian strip maturation. Collectively, these mechanisms synchronize developmental differentiation and transcriptome reprogramming for maintaining K+ homeostasis and optimizing nutrient foraging by roots.