Secreted CLAVATA3/EMBRYO SURROUNDING REGION (CLE) peptide ligands dimension the stem cell niche of Arabidopsis shoot meristems by signalling through redundant and cross-compensating CLAVATA1 (CLV1)-type receptor kinases. In the root meristem, the CLV1 homologues BARELY ANY MERISTEM 1 (BAM1) and BAM2 drive CLE13/16-mediated formative divisions that produce the ground tissue layers. Here we report that BAM1/2 are also required to initiate the vascular phloem lineage and that cross-compensation between CLV1-type receptors as observed in the shoot does not operate similarly in the root. Rather, we find that BAM3-mediated CLE45 signalling antagonizes BAM1/2-mediated CLE11/12/13 signalling in the phloem initials but not in the ground tissue. We further observe spatiotemporally contrasting CLE signalling requirements for phloem initiation and differentiation, which are shaped by the SHORT ROOT (SHR) pathway. Our findings thus suggest an intricate quantitative interplay between distinct and antagonistic CLE signalling pathways that organizes tissue layer formation in the Arabidopsis root meristem.