Cell-cycle-driven epigenetic resetting maintains meristematic cell fate for shoot branching

Cell proliferation generally promotes differentiation, whereas proliferative quiescence maintains stem cell identity-a paradigm well-established in adult mammalian stem cells. Here we report that in Arabidopsis bud precursor cells, meristematic cell fate maintenance depends on active cell-cycle progression. We identify two opposing mechanisms that balance trimethylated histone H3 Lys27 levels to regulate transcription of the shoot meristem marker gene SHOOT MERISTEMLESS (STM). On one hand, two classes of transcription factors recruit Polycomb repressive complex 2 (PRC2) to epigenetically silence STM. On the other hand, cell proliferation reduces trimethylated histone H3 K27 levels to counteract this silencing. We demonstrate that inhibiting cell division suppresses STM expression and promotes differentiation. The interplay between these forces establishes a cell-cycle-coupled epigenetic resetting mechanism that sustains pluripotency. This cell fate switch is bistable; both modelling and experimental data confirm that prolonged quiescence triggers irreversible differentiation. We propose that in plants, sequence-dependent PRC2 recruitment enables precise silencing of fate-determining genes, while cell proliferation maintains pluripotency through periodic resetting of epigenetic marks.