Perception of root‐active CLE peptides requires CORYNE function in the phloem vasculature

Abstract

Arabidopsis root development is orchestrated by signaling pathways that consist of different CLAVATA 3/ EMBRYO SURROUNDING REGION ( CLE ) peptide ligands and their cognate CLAVATA ( CLV ) and BARELY ANY MERISTEM ( BAM ) receptors. How and where different CLE peptides trigger specific morphological or physiological changes in the root is poorly understood. Here, we report that the receptor‐like protein CLAVATA 2 ( CLV 2) and the pseudokinase CORYNE ( CRN ) are necessary to fully sense root‐active CLE peptides. We uncover BAM 3 as the CLE 45 receptor in the root and biochemically map its peptide binding surface. In contrast to other plant peptide receptors, we found no evidence that SOMATIC EMBRYOGENESIS RECEPTOR KINASE ( SERK ) proteins act as co‐receptor kinases in CLE 45 perception. CRN stabilizes BAM 3 expression and thus is required for BAM 3‐mediated CLE 45 signaling. Moreover, protophloem‐specific CRN expression complements resistance of the crn mutant to root‐active CLE peptides, suggesting that protophloem is their principal site of action. Our work defines a genetic framework for dissecting CLE peptide signaling and CLV / BAM receptor activation in the root. image The plant membrane receptor kinase BAM 3 directly senses/binds the CLE 45 peptide ligand with its leucine‐rich repeat ectodomain, but BAM 3 activation does not rely on SERK family co‐receptor kinases. Moreover, different CLE peptides are able to suppress root growth via inhibition of protophloem development, a process that requires the presence of the pseudokinase CRN . The Arabidopsis receptor kinase BAM 3 is a genuine receptor of the CLE 45 peptide ligand and likely acts independent of SERK co‐receptors. In general, CLE peptides suppress root growth by preventing protophloem differentiation, which requires local activity of the receptor pseudokinase CRN . CRN activity promotes CLE 45 sensitivity of developing protophloem by post‐translational stabilization of BAM 3.