Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state

Abstract

Reprogramming of epigenetic states in gametes and embryos is essential for correct development in plants and mammals1. 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 next2-4. 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 embryos5-7.

Physical coupling of activation and derepression activities to maintain an active transcriptional state at FLC

“…2G) (29), whereas lack of ELF6 increased H3K27me3 (Fig. 2H) (1). As expected from the coupling of SDG8 and ELF6, loss of the H3K36 methyltransferase not only caused reduction of H3K36me3 but also increased H3K27me3 levels at FLC, and similarly, lack of ELF6 decreased H3K36me3 (Fig.…”

“…1B). ELF6 is an H3K27me3 demethylase in Arabidopsis shown to prevent inheritance of the vernalized state to the next generation through its demethylase activity (1). To confirm this interaction, ELF6:GFP and SDG8:Flag were transiently coexpressed in Nicotiana benthamiana by Agrobacterium infiltration.…”

“…Both SDG8 and ELF6 are FLC activators in flowering time regulation (1,14,16,29,38). To address whether SDG8 and ELF6 are functional in the same genetic pathway, the loss-of-function mutants were combined together by crossing.…”

“…Transcriptional states are induced by internal developmental signals or triggered by environmental conditions and are then epigenetically maintained through many cell divisions. Considerable evidence suggests that opposing histone modifications mark different transcriptional states (1)(2)(3)(4)(5)(6). However, there is still great debate as to how histone-based transcriptional states are initially established and maintained through development (7,8).…”

A comparative transcriptomic approach to understanding the formation of cork

“…FLC (FLOWERING LOCUS C) is a floral repressor that integrates vernalization responses (Sheldon et al 2000) and in perennial trees an FLC-like gene has also been highlighted as a candidate for bud dormancy regulation (Porto et al 2015). FLC regulation is basically performed by chromatin remodelling since FLC expression is epigenetically regulated (Shindo et al 2006;Jung et al 2013;Crevillén et al 2014). Taking into account that FLC has a role in xylem differentiation (Sibout et al 2008), it can be surmised that FLC also has a function in phellem development.…”