Antagonistic Roles for H3K36me3 and H3K27me3 in the Cold-Induced Epigenetic Switch at Arabidopsis FLC

Abstract

SummaryPosttranslational modifications of histone tails are an important factor regulating chromatin structure and gene expression. Epigenetic memory systems have been predicted to involve mutually exclusive histone modifications that, through positive feedback mechanisms, generate bistable states [1, 2]. How the states are interconverted is not understood, and whether the histone modifications are sufficient for epigenetic memory is still greatly debated [3]. We have exploited the process of vernalization, the slow quantitative epigenetic silencing of Arabidopsis FLC induced by cold, to detail with fine temporal and spatial resolution the dynamics of histone modifications during an epigenetic switch. The profiles of H3K36me3, H3K4me3, and H3K4me2 at FLC throughout the vernalization process were compared to H3K27me3, which accumulates at a local nucleation region during the cold and spreads across the locus on return to the warm [2]. We find for many phases of the vernalization process that H3K36me3 and H3K27me3 show opposing profiles in the FLC nucleation region and gene body, that H3K36me3 and H3K27me3 rarely coexist on the same histone tail, and that this antagonism is functionally important. A lack of H3K36me3 results in a fully silenced state at FLC even in the absence of cold. We therefore propose that H3K36me3 is the opposing modification to H3K27me3 in the Polycomb-mediated silencing of FLC. However, the lack of an absolute mirror profile predicted from modeling suggests that their antagonistic roles contribute a necessary, but not sufficient, component of the mechanism enabling switching between and inheritance of epigenetic states.

Divergence of annual and perennial species in the Brassicaceae and the contribution of cis‐acting variation at FLC orthologues

“…2011; Yang et al . 2014) (Fig. S11, Supporting information) as well as duplicated regions showing homology to the VRE (Sung et al .…”

“…One of the common SNP frequency peaks was detected in a region homologous to the nucleation region (Yang et al . 2014), and the second was present upstream of the VRE (Sung et al . 2006) (Figs 5A, S19 and S20, Supporting information).…”

“…Later studies demonstrated that the 5′ end of intron 1 overlaps with a region referred to as the nucleation region, at which H3K27 accumulates most rapidly and to high levels during vernalization (Yang et al . 2014). The same region contains two RY elements which act as binding sites of the transcriptional repressor VAL1 that nucleates silencing at the FLC locus by interacting with the apoptosis‐ and splicing‐associated protein (ASAP) complex and maybe Polycomb Repressive Complex 1 (PRC1) (Qüesta et al .…”

“…2002); nucleation region is the sequence homologous to the region showing elevated H3K27me3 before vernalization in Arabidopsis (Yang et al . 2014); COLDAIR is the regions homologous to the COLDAIR RNA encoding region (Heo & Sung 2011); Vernalization Responsive Element (VRE) indicates the region homologous to the VRE of A. thaliana identified in (Sung et al . 2006)).…”

“…S11 Alignment of the A. montbretiana and A. alpina region homologous to the nucleation region in A. thaliana defined by the ChIP primers from (Yang et al . 2014). …”