The accumulation of the mitotic B2-type CDK is tightly controlled by multiple pathways in Arabidopsis roots. Root growth depends on cell proliferation in the apices, which determines the root meristem size. The expression of B2-type cyclin-dependent kinase (CDKB2) is known to be restricted to dividing cells in the meristematic region, and therefore, the mechanisms controlling CDKB2 accumulation may be associated with those determining the meristem size. We investigated how CDKB2 expression is controlled in distinct zones of Arabidopsis roots. We found that CDKB2;1 expression was induced by a member of the PLETHORA (PLT) family of transcription factors, which are known to mediate auxin signaling and maintain the undifferentiated state of meristematic cells. When the root meristem was treated with an auxin antagonist, the CDKB2;1 level was reduced not only by transcriptional suppression but also by proteasome-mediated protein degradation. This indicates that auxin promotes CDKB2 accumulation at both mRNA and protein levels in the meristem. In the elongation and differentiation zones, on the other hand, neither the ubiquitin-proteasome system nor the PLT-mediated transcriptional regulation is associated with CDKB2;1 accumulation. Both CDKB2;1 and HIGH PLOIDY2 (HPY2), a SUMO E3 ligase, were ectopically accumulated in the stele when treated with exogenous auxin, suggesting the possibility that CDKB2;1 accumulation is dependent on HPY2-mediated sumoylation, which is usually maintained by a higher auxin level in the meristem. Our results demonstrate that the CDKB2 level is tightly controlled by multiple pathways to maintain the mitotic activity in developing roots.