Recent years have witnessed great advance in our mechanistic understanding of vernalization in overwintering plants. The FLC locus, the hub of vernalization network, is epigenetically silenced by polycomb-mediated histone methylation during vernalization, which thereby removes the suppression on the FT locus for flowering to occur. We know that during embryogenesis this histone methylation of FLC is reset to ensure a requirement for vernalization in each generation but little is known about the resetting mechanism.
Pedro Crevillen and colleagues now report that an H3K27me3 demethylase, ELF6, plays a critical role in the FLC resetting (Nature, Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state). They isolated an Arabidopsis mutant (elf6-5) with full silencing of FLC by vernalization but partial restoration of FLC expression in the following generation. The resetting mutant shows earlier flowering and reduced FLC expression. Genetic mapping narrowed down on a non-synonymous causal mutation on gene ELF6. FLC expression pattern analyses in elf6-5 and the wild type supported the idea that ELF6 promoted the expression of FLC as the embryo developed.
To understand how ELF6 regulates FLC expression, they tested the potential mediator, COOLAIR and siRNAs, neither of which seemed to be involved in the process. Instead, using an in vivo histone demethylation assay, they found the wild-type ELF6 had H3K27 demethylation activity in tobacco leaves, but the mutant elf6 showed reduced activity. In vivo experiments utilizing chromatin immunoprecipitation indicated FLC H3K27me3 was indeed reset (demethylated) in siliques of the vernalized wild type but not fully reset in elf6-5. Also in the next-generation progeny after vernalization, the elf6-5 seedlings showed a higher H3K27me3 methylation of FLC than the wild type. Therefore, without an intact ELF6, the demethylation resetting of FLC would be impaired, resulting in the inheritance of a partially vernalized state.
Mammalian embryos also harness a similar mechanism for epigenetic reprogramming. This study thus indicated an ancient role for H3K27 demethylation in embryonic epigenetic reprogramming shared by plants and animals.