Conserved DNA architect couples chloroplast development to cell cycle in developing cotyledons.

Light orchestrates cotyledon greening and growth by coordinating chloroplast development with cell division and expansion, yet the molecular integrator of these processes remains unknown. Here we identify RDE (REGULATOR OF DG1 EXPRESSION), a conserved DNA architectural factor that synchronizes thylakoid protein complex biogenesis during chloroplast development with the G1-S transition of cell cycle progression in Arabidopsis thaliana. RDE mediates promoter DNA bending to sequester DPa in stable nucleoprotein complexes, precluding DPa-E2Fa heterodimer formation. This repression mechanism controls both S-phase genes and EMBRYO-DEFECTIVE (EMB) loci encoding chloroplast RNA-binding proteins involved in synthesis of plastid-encoded thylakoid proteins. The RDE-mediated repression is light relieved, enabling concurrent etioplast-to-chloroplast differentiation and G1-S transition that drives endoreplication-dependent cell expansion for cotyledon greening and growth. This RDE-E2Fa-DPa module is conserved across green plants, from unicellular algae to angiosperms. Our work identifies a chloroplast developmental rheostat that evolutionarily tethers organelle biogenesis to proliferative growth, a synchronization mechanism vital for photosynthetic eukaryote adaptation.