Transcription in Pronuclei and One- to Four-Cell Embryos Drives Early Development in a Nematode

Background: A long-standing view of development is that transcription is silenced in the oocyte until early divisions in the embryo. The point at which major transcription is reactivated varies between organisms, but is usually after the two-cell stage. However, this model may not be universal. Results: We used RNA-seq and exploited the protracted development of the parasitic nematode Ascaris suum to provide a comprehensive time course of mRNA expression, degradation, and translation during early development. Surprisingly, we find that similar to 4,000 genes are transcribed prior to pronuclear fusion and in the one-to four-cell embryos. Intriguingly, we do not detect maternal contribution of many orthologs of maternal C. elegans mRNAs, but instead find that these are newly transcribed in the A. suum zygote prior to pronuclear fusion. Ribosome profiling demonstrates that, in general, early embryonic mRNAs are not stored for subsequent translation, but are directly translated after their synthesis. The role of maternally contributed and zygotically transcribed genes differs between the nematodes A. suum and C. elegans despite the fact that the two nematodes appear to exhibit highly similar morphological patterns during early development. Conclusions: Our study indicates that major transcription can occur immediately after fertilization and prior to pronuclear fusion in metazoa, suggesting that newly transcribed genes appear to drive A. suum early development. Furthermore, the mechanisms used for controlling the timing of the expression of key conserved genes has been altered between the two nematodes, illustrating significant plasticity in the regulatory networks that play important roles in developmental outcomes in nematodes.