RETINOBLASTOMA-RELATED PROTEIN controls the transition to autotrophic plant development

Seedling establishment is a crucial phase during plant development when the germinating heterotrophic embryo switches to autotrophic growth and development. Positive regulators of embryonic development need to be turned off, while the cell cycle machinery is activated to allow cell cycle entry and organ primordia initiation. However, it is not yet understood how the molecular mechanisms responsible for the onset of cell division, metabolism changes and cell differentiation are coordinated during this transition. Here, we demonstrate that the Arabidopsis thaliana RETINOBLASTOMA-RELATED protein (RBR) ortholog of the animal tumor suppressor retinoblastoma (pRB) not only controls the expression of cell cycle-related genes, but is also required for persistent shut-down of late embryonic genes by increasing their histone H3K27 trimethylation. Seedlings with reduced RBR function arrest development after germination, and stimulation with low amounts of sucrose induces transcription of late embryonic genes and causes ectopic cell division. Our results suggest a model in which RBR acts antagonistically to sucrose by negatively regulating the cell cycle and repressing embryonic genes. Thus, RBR is a positive regulator of the developmental switch from embryonic heterotrophic growth to autotrophic growth. This establishes RBR as a new integrator of metabolic and developmental decisions.