Conserved and differentiated functions of CIK receptor kinases in modulating stem cell signaling in Arabidopsis

Abstract

The shoot apical meristem (SAM) and root apical meristem (RAM) act as pools of stem cells that give rise to aboveground and underground tissues and organs in higher plants, respectively. The CLAVATA3 (CLV3)-WUSCHEL (WUS) negative-feedback loop acts as a core pathway controlling SAM homeostasis, while CLV3/EMBRYO SURROUNDING REGION (ESR) 40 (CLE40) and WUSCHEL-RELATED HOMEOBOX5 (WOX5), homologs of CLV3 and WUS, direct columella stem cell fate. Moreover, CLV3 INSENSITIVE KINASES (CIKs) have been shown to be essential for maintaining SAM homeostasis, whereas whether they regulate the distal root meristem remains to be elucidated. Here, we report that CIKs are indispensable for transducing the CLE40 signal to maintain homeostasis of the distal root meristem. We found that the cik mutant roots displayed disrupted quiescent center and delayed columella stem cell (CSC) differentiation. Biochemical assays demonstrated that CIKs interact with ARABIDOPSIS CRINKLY4 (ACR4) in a ligand-independent manner and can be phosphorylated by ACR4 in vitro. In addition, the phosphorylation of CIKs can be rapidly induced by CLE40, which partially depends on ACR4. Although CIKs act as conserved and redundant regulators in the SAM and RAM, our results demonstrated that they exhibit differentiated functions in these meristems.