Abstract
Maternal-zygotic transition (MZT) is critical for the developmental control handed from maternal products to newly synthesized zygotic genome in the earliest stage of embryogenesis. However, the spatiotemporal dynamic regulation of MZT by maternal factors is largely unknown. Here, we reported a novel maternal factor, DCAF13, which was highly expressed in growing oocyte nucleolus and had key maternal effects on oocyte and zygotic chromatin tightness during maternal to zygotic transition. DCAF13 specifically deleted in oocytes resulted in loose chromatin structure in fully grown germinal vesicle oocytes. Despite normal nuclear maturation in maternal DCAF13-deleted oocytes, the chromosomes at MII stage were not properly condensed. Consequently, the nuclear and nucleolar structure reorganized abnormally, and transcription was inactive in zygotic embryos. RNA-seq analysis of MII oocytes and 2-cell embryos demonstrated that the transcriptomes between knockout and control oocyte were similar, but the maternal DCAF13 deleted two-cell embryos showed a significant decrease in transcription. In addition, the maternal DCAF13-deleted embryos displayed arrest at the two-cell stage, which could not be rescued by injecting flag-Dcaf13 mRNA in the zygote. This revealed that DCAF13 was a unique maternal effect factor regulating the nucleolus.
Highlights
In vertebrates, maternal-zygotic transition (MZT) is not a one-stage process, but a process that is active from fertilization to the step when the zygotic genome is fully activated, and maternal mRNAs are completely degraded[1]
We found that the Dcaf13fl/fl;Zp3-Cre oocytes did not show any defect in GVBD or PB1 emission (Fig. 1b)
The development depends on maternal protein and RNA stored by oocytes before zygotic genome activation (ZGA), which occurs at the one-cell stage[15]
Summary
Maternal-zygotic transition (MZT) is not a one-stage process, but a process that is active from fertilization to the step when the zygotic genome is fully activated, and maternal mRNAs are completely degraded[1]. Successful zygotic genome activation (ZGA) is required for further embryo development, failure of which causes growth arrest. Embryos derived from denucleated oocytes fail to develop beyond the two-cell stage, suggesting that the oocyte nucleus has a pivotal role in early embryonic development[10]. These studies suggest that the nucleus/nucleolus morphology and chromatin configuration need to be changed to adapt to the gradually recovered transcription during MZT. In this mouse model, the majority of the oocytes fail to develop to the preovulatory stage and became apoptotic. DCAF13 binds with the nucleolar protein fibrillarin and is involved in the processing of 18S rRNA during oocyte growth[13]
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