Abstract
The earliest stages of animal development are controlled by maternally deposited mRNA transcripts and proteins. Once the zygote is able to transcribe its own genome, maternal transcripts are degraded, in a tightly regulated process known as the maternal to zygotic transition (MZT). While this process has been well-studied within model species, we have little knowledge of how the pools of maternal and zygotic transcripts evolve. To characterize the evolutionary dynamics and functional constraints on early embryonic expression, we created a transcriptomic dataset for 14 Drosophila species spanning over 50 million years of evolution, at developmental stages before and after the MZT, and compared our results with a previously published Aedes aegypti developmental time course. We found deep conservation over 250 million years of a core set of genes transcribed only by the zygote. This select group is highly enriched in transcription factors that play critical roles in early development. However, we also identify a surprisingly high level of change in the transcripts represented at both stages over the phylogeny. While mRNA levels of genes with maternally deposited transcripts are more highly conserved than zygotic genes, those maternal transcripts that are completely degraded at the MZT vary dramatically between species. We also show that hundreds of genes have different isoform usage between the maternal and zygotic genomes. Our work suggests that maternal transcript deposition and early zygotic transcription are remarkably dynamic over evolutionary time, despite the widespread conservation of early developmental processes.
Highlights
Most early developmental processes, such as rapid cleavage cycles and the establishment of body axes, are shared across multicellular animals, but the extent to which the mechanisms and the genes involved are shared remains an open question.Throughout the animal kingdom, the first stages of development are controlled by mRNA transcripts and proteins deposited by the mother during oogenesis
This is accomplished through a precise and elegant series of regulatory steps, in which the zygotic genome is transcriptionally activated while maternal transcripts are degraded, in a process known as the maternal to zygotic transition
Transcript levels at stage 5 are a function of multiple processes: maternal RNA deposition that occurred during oogenesis, multiple embryonic degradation pathways, which themselves may be activated either maternally or zygotically [53,54], and early zygotic transcription
Summary
Most early developmental processes, such as rapid cleavage cycles and the establishment of body axes, are shared across multicellular animals, but the extent to which the mechanisms and the genes involved are shared remains an open question.Throughout the animal kingdom, the first stages of development are controlled by mRNA transcripts and proteins deposited by the mother during oogenesis. Genetic control is subsequently transferred from the maternal genome to the zygotic genome This is accomplished through a precise and elegant series of regulatory steps, in which the zygotic genome is transcriptionally activated while maternal transcripts are degraded, in a process known as the maternal to zygotic transition This handoff between mother and zygote has the appearance of a functional logic that dictates which genome is in control. The maternal and zygotic genomes are able to coordinate during the MZT to such a degree that the transcript levels of these genes can be relatively constant, despite the transition between genomes of origin for these transcripts
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