Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state

Reprogramming of epigenetic states in gametes and embryos is essential for correct development in plants and mammals(1). In plants, the germ line arises from somatic tissues of the flower necessitating erasure of chromatin modifications accumulated at specific loci during development or in response to external stimuli. If this occurs inefficiently it can lead to epigenetic states being inherited from one generation to the next(2-4). However, in most cases accumulated epigenetic modifications are efficiently erased before the next generation. An important example of epigenetic reprogramming in plants is the resetting of expression of the Arabidopsis thaliana floral repressor FLC locus. FLC is epigenetically silenced by prolonged cold in a process called vernalization. However, the locus is reactivated prior to completion of seed development to ensure a vernalization requirement every generation. In contrast to our detailed understanding of the Polycomb-mediated epigenetic silencing induced by vernalization, little is known about the mechanism involved in the re-activation of FLC. Here we show that a hypomorphic mutation in the jumonji domain protein ELF6 impaired the reactivation of FLC in reproductive tissues, leading to inheritance of a partially vernalized state. ELF6 has H3K27me3 demethylase activity and the mutation reduced this enzymatic activity in planta. Consistent with this, H3K27me3 levels at the FLC locus stayed higher and FLC expression remained lower, than in the wild type in the following generation. Our data reveal an ancient role for H3K27 demethylation in the reprogramming of epigenetic states in plant and mammalian embryos(5-7).