Combinations of maternal-specific repressive epigenetic marks in the endosperm control seed dormancy

Abstract

Polycomb Repressive Complex 2 (PRC2)-mediated trimethylation of histone H3 on lysine 27 (H3K27me3) and methylation of histone 3 on lysine 9 (H3K9me) are two repressive epigenetic modifications that are typically localized in distinct regions of the genome. For reasons unknown, however, they co-occur in some organisms and special tissue types. In this study, we show that maternal alleles marked by H3K27me3 in the Arabidopsis endosperm were targeted by the H3K27me3 demethylase REF6 and became activated during germination. In contrast, maternal alleles marked by H3K27me3, H3K9me2, and CHGm were protected from REF6 targeting and remained silenced. Our study unveils that combinations of different repressive epigenetic modifications time a key adaptive trait by modulating access of REF6.

A histone deacetylase complex establishes a transgenerationally inherited maternal epigenetic state controlling progeny seed dormancy

“…This gene set includes three transcription factors associated with senescence: ORESERA1 ( ORE1 ) 25 , WRKY75 26 and NAC046 27 , a close relative of ORE1. ORE1 expression is also repressed by excess H3K27me3 in plants lacking the H3K27me3 demethylase REF6 28 and we found the same is true for WRKY75 and NAC046 in the endosperm (Fig.5C, Supplementary Fig.5C and ref 11 ). Interestingly REF6 has already been shown to repress seed dormancy 11, 29 .…”

“…ORE1 expression is also repressed by excess H3K27me3 in plants lacking the H3K27me3 demethylase REF6 28 and we found the same is true for WRKY75 and NAC046 in the endosperm (Fig.5C, Supplementary Fig.5C and ref 11 ). Interestingly REF6 has already been shown to repress seed dormancy 11, 29 . At these loci H3K27me3 is established during the coenocytic phase of endosperm development when VEL3 is expressed, and the presence of H3K27me3 at ORE1, WRKY75 and NAC046 in the mature endosperm requires VEL3 (Fig.5D).…”

“…5C, Supplementary Fig. 5C and ref 11 ). Interestingly REF6 has already been shown to repress seed dormancy 11,29 .…”

“…Although imprinted genes can be expressed at any stage of seed development and germination, the timing of chromatin remodelling events that control dormancy and germination is less clear. The H3K27me3 demethylase REF6 is required for gene activation during germination 11 and imprinting can also be lost during dormancy loss in the mature seed 12 . But some genetic evidence suggests that some chromatin modellers act earlier in endosperm development, or even in the central cell to affect seed dormancy 11 .…”

“…The H3K27me3 demethylase REF6 is required for gene activation during germination 11 and imprinting can also be lost during dormancy loss in the mature seed 12 . But some genetic evidence suggests that some chromatin modellers act earlier in endosperm development, or even in the central cell to affect seed dormancy 11 . Here we show that mothers maintain progeny dormancy via inheritance of dormancy-inducing epi-alleles in the endosperm.…”