Composition and regulation of maternal and zygotic transcriptomes reflects species-specific reproductive mode

Early embryos contain mRNA transcripts expressed from two distinct origins; those expressed from the mother's genome and deposited in the oocyte (maternal) and those expressed from the embryo's genome after fertilization (zygotic). The transition from maternal to zygotic control occurs at different times in different animals according to the extent and form of maternal contributions, which likely reflect evolutionary and ecological forces. Maternally deposited transcripts rely on post-transcriptional regulatory mechanisms for precise spatial and temporal expression in the embryo, whereas zygotic transcripts can use both transcriptional and post-transcriptional regulatory mechanisms. The differences in maternal contributions between animals may be associated with gene regulatory changes detectable by the size and complexity of the associated regulatory regions.

We have used genomic data to identify and compare maternal and/or zygotic expressed genes from six different animals and find evidence for selection acting to shape gene regulatory architecture in thousands of genes. We find that mammalian maternal genes are enriched for complex regulatory regions, suggesting an increase in expression specificity, while egg-laying animals are enriched for maternal genes that lack transcriptional specificity.

We propose that this lack of specificity for maternal expression in egg-laying animals indicates that a large fraction of maternal genes are expressed non-functionally, providing only supplemental nutritional content to the developing embryo. These results provide clear predictive criteria for analysis of additional genomes.