A CLE-CIK signaling module controls columella root cap formation in Arabidopsis

CLAVATA3 (CLV3)/EMBRYO SURROUNDING REGION-RELATED (CLE) peptides play essential roles during plant development. Their biological functions closely correlate with their spatiotemporal expression patterns. Root cap is a critical protective and sensory organ of root. How CLEs regulate root cap development has not been elucidated. We identified a group of peptides, CLE11/12/13 with expression in the root cap. The cle11/12/13 mutants exhibited reduced number of columella cell layers. Similar defects of columella cell layers were found in mutants of CLV3 INSENSITIVE RECEPTOR KINASE 1/4 (CIK1/4). Phosphorylation levels of CIK1/4 were enhanced upon CLE11/12/13 treatment. Genetic analyses revealed that CLE11/12/13 and CIK1/4 co-regulate columella root cap formation. The expression of columella stem cell (CSC) marker J2341 in cik1/4 was reduced, and the cle11/12/13 and cik1/4 mutants showed decreased CSC division activity. Furthermore, the mutant fez-2 displayed similarly reduced columella cell layers, and induced overexpression of FEZ can partially restore columella cell layer defect of the cik1/4 mutant. Our work clarifies that the CLE11/12/13-CIK1/4 signaling module acts upstream of FEZ to promote CSC division activity and is essential for columella root cap morphogenesis. These findings not only expand the biological roles of peptide-receptor kinase signaling but also establish an association with the critical factors to deepen our understanding of columella root cap development.