Embryonic transcription is controlled by maternally defined chromatin state.

Saartje Hontelez,Ozren Bogdanovic,Gert Jan C Veenstra,Ila Van Kruijsbergen,Simon J Van Heeringen,Georgios Georgiou,Ryan Lister

doi:10.1038/ncomms10148

Abstract

Histone-modifying enzymes are required for cell identity and lineage commitment, however little is known about the regulatory origins of the epigenome during embryonic development. Here we generate a comprehensive set of epigenome reference maps, which we use to determine the extent to which maternal factors shape chromatin state in Xenopus embryos. Using α-amanitin to inhibit zygotic transcription, we find that the majority of H3K4me3- and H3K27me3-enriched regions form a maternally defined epigenetic regulatory space with an underlying logic of hypomethylated islands. This maternal regulatory space extends to a substantial proportion of neurula stage-activated promoters. In contrast, p300 recruitment to distal regulatory regions requires embryonic transcription at most loci. The results show that H3K4me3 and H3K27me3 are part of a regulatory space that exerts an extended maternal control well into post-gastrulation development, and highlight the combinatorial action of maternal and zygotic factors through proximal and distal regulatory sequences.

Highlights

Histone-modifying enzymes are required for cell identity and lineage commitment, little is known about the regulatory origins of the epigenome during embryonic development
Little is known about the origin and specification of the epigenome in embryonic development of vertebrates, which is essential for understanding physiological cell lineage commitment and differentiation
In addition we generated pre-mid-blastula transition (MBT) maps for three histone modifications (H3K4me[3], H3K9ac and H3K27me3) and single-base resolution DNA methylome maps using whole-genome bisulfite sequencing of blastula and gastrula embryos (Fig. 1; Supplementary Fig. 1)

Summary

Introduction

Histone-modifying enzymes are required for cell identity and lineage commitment, little is known about the regulatory origins of the epigenome during embryonic development. Using a-amanitin to inhibit zygotic transcription, we find that the majority of H3K4me3- and H3K27me3-enriched regions form a maternally defined epigenetic regulatory space with an underlying logic of hypomethylated islands. This maternal regulatory space extends to a substantial proportion of neurula stage-activated promoters. P300 recruitment to distal regulatory elements is largely under the control of zygotic factors This maternal-proximal and zygotic-distal dichotomy of gene regulatory sequences differentiates between early and late Wnt signalling target genes, suggesting that different levels of permissiveness are involved in temporal target gene selection

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Results

Conclusion