Targets and mechanisms of epigenetic regulation in the temperate cereal vernalisation process

Abstract

Vernalisation is a prolonged cold exposure that synchronises flowering with favourable seasonal conditions, protecting reproductive development from winter stress and optimising crop yields. By 'recording' winter, this biological process displays memory and becomes progressively more difficult to reverse. In the well-studied model Arabidopsis, vernalisation epigenetically silences the gene locus of the floral repressor FLC. Temperate cereals, including crops such as wheat and barley, respond to a similar vernalisation cue with a memory property and recent functional studies also support an epigenetic mechanism. Current evidence points to the flowering promoter VRN1 as the primary site for storing this memory. Because vernalisation in cereals appears to rely on epigenetic activation of VRN1, rather than repression as in Arabidopsis, the specific histone marks responsible for storing this epigenetic memory are possibly different. This highlights the need for further research to identify the specific genes and histone modifications involved, and to fully elucidate the mechanisms underlying vernalisation memory in cereals. The goal of this review is to synthesise recent advances in our understanding of the epigenetic regulation of vernalisation in temperate cereals. Therefore, this review focuses on the roles of key genes such as VRN1, VRN3, and ODDSOC2, and examines the dynamic chromatin landscape associated with vernalisation-induced flowering. In particular, we investigate the possible interplay of chromatin marks involved in the epigenetic activation of VRN1. By synthesising current knowledge and highlighting unresolved questions, this review aims to provide a framework for future research in the field of cereal vernalisation memory.

Keywords: VRN1; devernalisation; histone modification; temperate cereals; vernalisation.

Figure 1

Structural domain composition VRN1, VRN2, VRN3, and ODDSOC2. Schematic representation of the structural domains present in VRN1, VRN2, VRN3, and ODDSOC2, showing the arrangement of MADS, intervening (I), keratin-like (K), C-terminal, and PEBP domains to highlight differences in domain composition among these key flowering regulators from Brachypodium distachyon. Created in BioRender. Daneels, T. (2025) https://BioRender.com/lo4b3yy.

Figure 2

Genetic and epigenetic network controlling vernalisation and flowering in temperate cereals. This figure illustrates the genetic and epigenetic regulation of flowering in temperate cereals in response to cold and light: before vernalisation, VRN1 is repressed by high H3K27me3 (via PRC2/EZL1), as well as by the pre-vernalisation repressors RVR1 and JMJ1, with JMJ1 demethylating H3K4 to further silence VRN1; this maintains active VRN2 and ODDSOC2, which keep VRN3 inhibited. During and after cold exposure, VRN1 is activated through loss of H3K27me3 and gain of H3K4me3, leading to stable expression and winter memory; VRN1 then represses VRN2 and ODDSOC2, releasing VRN3 from inhibition. VRN3 activation is marked by increased H3K4me3, especially under long days. ODDSOC2 repression involves increased H3K27me3 in Brachypodium, while in wheat and barley, its downregulation is associated with reduced H3K4me3 and is mediated by VRN1. These coordinated genetic and chromatin changes, regulated by EZL1, RVR1, and JMJ1, integrate cold and photoperiod signals to precisely control flowering time. Created in BioRender. Daneels, T. (2025) https://BioRender.com/0z70j0s.

Figure 3

Epigenetic activation VRN1 locus by vernalisation. The figure depicts the epigenetic regulation of the VRN1 locus during vernalisation in temperate cereals as a continuous process. Before cold exposure, VRN1 chromatin is compact and enriched in the repressive mark H3K27me3 (red), keeping the gene silent. During prolonged cold, H3K27me3 levels gradually decrease while activating marks such as H3K4me3 (green) and H3K27Ac or H3K9Ac (blue) accumulate, leading to chromatin opening and VRN1 activation. After vernalisation, in warm conditions, VRN1 remains actively transcribed with sustained H3K4me3, H3K27Ac, H3K9Ac, and H3K36me3 marks, which stabilise expression and prevent re-silencing. The transcription factor VRT2 regulates the PRC2 component SUZ12 to block re-deposition of H3K27me3, ensuring the vernalised, active state is maintained. Colours: red, H3K27me3; green, H3K4me3; blue, acetylation. Created in BioRender. Daneels, T. (2025) https://BioRender.com/v14g358.