Abstract
Oocytes are arrested for long periods of time in the prophase of the first meiotic division (prophase I). As chromosome condensation poses significant constraints to gene expression, the mechanisms regulating transcriptional activity in the prophase I-arrested oocyte are still not entirely understood. We hypothesized that gene expression during the prophase I arrest is primarily epigenetically regulated. Here we comprehensively define the Drosophila female germ line epigenome throughout oogenesis and show that the oocyte has a unique, dynamic and remarkably diversified epigenome characterized by the presence of both euchromatic and heterochromatic marks. We observed that the perturbation of the oocyte's epigenome in early oogenesis, through depletion of the dKDM5 histone demethylase, results in the temporal deregulation of meiotic transcription and affects female fertility. Taken together, our results indicate that the early programming of the oocyte epigenome primes meiotic chromatin for subsequent functions in late prophase I.
Highlights
Oocytes are arrested for long periods of time in the prophase of the first meiotic division
Our results indicate that the programming of the Drosophila oocyte epigenome during early oogenesis controls, several hours later, the transcriptional reactivation of meiotic chromatin
We show that the disruption of the oocyte epigenome, mainly through increased levels of histone H3 lysine 4 trimethylation (H3K4me3), a euchromatic mark associated with the transcription start site of active genes[12,13], leads to significant defects in three main biological programs: (i) temporal control of gene expression; (ii) regulation of RNA polymerase II (RNAPII) levels in oocyte chromatin; and (iii) remodelling of the meiotic chromosomes in late prophase I
Summary
Oocytes are arrested for long periods of time in the prophase of the first meiotic division (prophase I). We show that the disruption of the oocyte epigenome, mainly through increased levels of histone H3 lysine 4 trimethylation (H3K4me3), a euchromatic mark associated with the transcription start site of active genes[12,13], leads to significant defects in three main biological programs: (i) temporal control of gene expression; (ii) regulation of RNA polymerase II (RNAPII) levels in oocyte chromatin; and (iii) remodelling of the meiotic chromosomes in late prophase I. The nature of these defects has a critical impact on meiotic completion and female fertility
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