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

The polycomb protein VERNALIZATION2 (VRN2) is a plant-specific subunit of the polycomb repressive complex 2 (PRC2), a conserved eukaryotic holoenzyme that represses gene expression by depositing the histone 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 positional and environmental cues. Here we show that VRN2 is enriched in hypoxic meristematic regions and emerging leaves of Arabidopsis under non-stressed conditions, and that vrn 2 mutants are larger than wild type, indicating that VRN2-PRC2 negatively regulates growth and development. This growth phenotype is caused by ectopic expression of genes that promote cell expansion, including many SAUR genes and other direct PIF transcription factor targets. Analysis of SAUR19 promoter activity and expression dynamics revealed that VRN2 is required to specifically repress these genes in the light. Moreover, we show that VRN2 is epistatic to PIF4, and directly binds and methylates histones of key loci in the PIF4 transcriptional network to provide robust light-responsive control of gene expression and growth. We propose that hypoxia-stabilised VRN2-PRC2 sets a conditionally repressed chromatin state at PIF-regulated hub genes early in leaf ontogeny coinciding with the cell division phase, and that this is required for enhancing their subsequent repression via a light-responsive signalling cascade as cells enter the expansion phase. Thus, we have identified VRN2-PRC2 as core component of a spatially regulated and developmentally encoded epigenetic mechanism that co-ordinates environment-responsive growth by facilitating light-triggered suppression of PIF signalling.