VEL-dependent polymerization maintains the chromatin association of Polycomb proteins for the switch to epigenetic silencing

Multivalent protein-chromatin interactions facilitated by higher-order protein assemblies are emerging as a crucial theme in eukaryotic gene regulation. However, understanding the underlying mechanisms in their functional context in vivo remains challenging. Arabidopsis VEL proteins assemble biomolecular condensates by head-to-tail polymerization. Here, we dissect the role of the VEL polymerization domains in conferring the epigenetic switch to Polycomb Repressive Complex 2 (PRC2) silencing at Arabidopsis FLOWERING LOCUS C (FLC). We show that VIN3 VEL polymerization produces higher order nuclear VIN3 assemblies in vivo, which promote multivalent chromatin association and efficient H3K27me3 nucleation. The VRN5 VEL domain, however, is genetically dispensable for silencing if a third homologue VEL1 is present. VRN5 VEL is unable to functionally replace VIN3 VEL but has a role in physically connecting VIN3 with PRC2. VIN3 chromatin association at FLC occurs independently of the DNA sequence-binding of the associated transcriptional repressor VAL1. This work reveals how VEL-dependent polymerization maintains the chromatin association of Polycomb proteins enabling the switch to epigenetic silencing.