Multifunctional polymerization domains determine the onset of epigenetic silencing in Arabidopsis

Cold-induced epigenetic silencing of Arabidopsis FLOWERING LOCUS C (FLC) requires the Polycomb Repressive Complex 2 and accessory proteins VIN3 and VRN5. VIN3 and VRN5 interact via head-to-tail VEL polymerization domains, but how these functionally contribute to the switch to an epigenetically silenced state remains poorly understood. Here, we determine that VIN3 VEL polymerization involves higher order nuclear VIN3 assemblies in vivo, promotes strong chromatin association and efficient H3K27me3 nucleation. However, we also show that the polymerization domains of VIN3 and VRN5 are not equivalent: VRN5 VEL domain is not required for silencing despite its role in physically connecting VIN3 with the PRC2 complex and VRN5 VEL is unable to functionally replace VIN3 VEL in vivo. Both VIN3 and VRN5 homologs are present throughout angiosperm species, suggesting a functional requirement for maintaining different polymerization modalities. This work reveals distinct roles for multifunctional polymerization domains of Polycomb accessory proteins underpinning the onset of epigenetic silencing.