Abstract
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.
| Original language | English |
|---|---|
| Article number | 5550 |
| Journal | Nature Communications |
| Volume | 16 |
| DOIs | |
| Publication status | Published Online - 1 Jul 2025 |
Funding
We thank Sheila Teves (University of British Columbia) for the assistance with low-salt chromatin extraction; Steven Henikoff (Fred Hutchinson Cancer Research Centre) for discussions on the MNase-seq data interpretation; Carlo Martins and Gerhard Saalbach (Proteomics Facility at John Innes Centre) for the mass spectrometry analysis service; Jitender Cheema (EMBL-EBI) for the help with processing raw sequencing data; Frédéric Berger (Gregor Mendel Institute, Vienna) for sharing the HTR5-GFP lines; and Richard Amasino for sharing the vrn1 fast neutron mutant. We also thank two previous lab members Clare Lister and Joshua Mylne for their assistance with the genomic VRN1 cloning and allelism tests respectively. This work was funded by grants from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme; EPISWITCH-833254 to CD; and 803326 to RCG. CD was also funded by Wellcome Trust grant 210654/Z/18/Z and a Royal Society Professorship RP\R1\180002. RCG and MJM are also supported by the UK Research and Innovation (UKRI) Engineering and Physical Sciences Research Council (EPSRC) under the UK Government’s guarantee scheme (grant EP/Z002028/1 awarded to RCG). MJM would like to acknowledge the Winton Programme for Physics of Sustainability for doctoral funding. JH is supported by the Herchel Smith Postdoctoral Fellowship Fund, and the EPSRC [grant number EP/X02332X/1] under the UKRI Postdoctoral Fellowships Guarantee Scheme [project TF-CHROM-LLPS]. This project made use of time on HPC granted via the UK High-End Computing Consortium for Biomolecular Simulation, HECBioSim (http://hecbiosim.ac.uk), supported by EPSRC (grant no. EP/X035603/1) to RCG.
All Science Journal Classification (ASJC) codes
- General Chemistry
- General Biochemistry,Genetics and Molecular Biology
- General Physics and Astronomy