Organogenesis relies on the coordination of cell proliferation with developmental programs. In meristems, where new plant organs initiate, the cell proliferation potential depends on stem cell regulators, but the mechanisms linking their local activity with the cell cycle machinery remain unknown. Here we show a positional gradient of G1 duration in the Arabidopsis root meristem spanning from ~2 h near the meristem boundary to more than 20 h in the early stem cell derivatives. Mutations in the stem cell regulatory PLETHORA (PLT) genes and the cell cycle RETINOBLASTOMA-RELATED 1 gene shortened G1 duration, abolishing the G1 duration gradient, whereas PLT2 overexpression increased G1 duration. Data-driven computer modelling supported the presence of an incoherent feed-forward loop. We found that PLT genes are drivers with simultaneous and opposing roles in maintaining stem cell activity and inhibiting G1 progression through a cascade involving the CDK inhibitor KRP5, a PLT target and RETINOBLASTOMA-RELATED 1. The G1 duration gradient is developmentally regulated and established after the emergence of lateral roots from the primary root and correlates with increased tolerance to genome damage. Our study establishes a previously undescribed proximal-distal G1 duration gradient during root development that is shaped by the balanced activity of stem cell maintenance and cell cycle regulators.