Cold-induced nucleosome dynamics linked to silencing of Arabidopsis FLC

Temperature influences nucleosome dynamics, and thus chromatin, to regulate gene expression. Such mechanisms underlie the epigenetic silencing of Arabidopsis FLOWERING LOCUS C (FLC) by prolonged cold. Here, we show a temperature-dependent transition in local chromatin structure at the H3K27me3 nucleation region, from a modality active for transcription to a state that can be Polycomb silenced. In vivo chromatin measurements and coarse-grained simulations at near-atomistic resolution show that the active transcription state is characterised by a highly dynamic nucleosome arrangement that exposes the FLC transcription start site (TSS). Cold exposure then changes the chromatin by reducing nucleosome dynamics and re-positioning the + 1 nucleosome, leading to transcriptional repression. This local chromatin transition partially depends on VERNALIZATION1 (VRN1), a non-sequence-specific DNA-binding protein. Loss of VRN1 results in hyperaccumulation of H2A.Z, more dynamic nucleosomes and an inability to accumulate H2Aub and H3K27me3. Our work highlights how local nucleosome dynamics link to chromatin structure transitions to integrate temperature inputs into epigenetic switching mechanisms in plants.