VRN2-PRC2 facilitates light-triggered repression of PIF signaling to coordinate growth in Arabidopsis

VERNALIZATION2 (VRN2) is a flowering plant-specific subunit of the polycomb-repressive complex 2 (PRC2), a conserved eukaryotic holoenzyme that represses gene expression by depositing the histone H3 lysine 27 trimethylation (H3K27me3) mark in chromatin. Previous work established VRN2 as an oxygen-regulated target of the N-degron pathway that may function as a sensor subunit connecting PRC2 activity to the perception of endogenous and environmental cues. Here, we show that VRN2 is enriched in the hypoxic shoot apex and emerging leaves of Arabidopsis, where it negatively regulates growth by establishing a stable and conditionally repressed chromatin state in key PHYTOCHROME INTERACTING FACTOR (PIF)-regulated genes that promote cell expansion. This function is required to keep these genes poised for repression via a light-responsive signaling cascade later in leaf development. Thus, we identify VRN2-PRC2 as a core component of a developmentally and spatially encoded epigenetic mechanism that coordinates plant growth through facilitating the signal-dependent suppression of PIF signaling.