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Abstract
The gene products that drive early development are critical for setting up developmental trajectories in all animals. The earliest stages of development are fueled by maternally provided mRNAs until the zygote can take over transcription of its own genome. In early development, both maternally deposited and zygotically transcribed gene products have been well characterized in model systems. Previously, we demonstrated that across the genus Drosophila, maternal and zygotic mRNAs are largely conserved but also showed a surprising amount of change across species, with more differences evolving at the zygotic stage than the maternal stage. In this study, we use comparative methods to elucidate the regulatory mechanisms underlying maternal deposition and zygotic transcription across species. Through motif analysis, we discovered considerable conservation of regulatory mechanisms associated with maternal transcription, as compared to zygotic transcription. We also found that the regulatory mechanisms active in the maternal and zygotic genomes are quite different. For maternally deposited genes, we uncovered many signals that are consistent with transcriptional regulation at the level of chromatin state through factors enriched in the ovary, rather than precisely controlled gene-specific factors. For genes expressed only by the zygotic genome, we found evidence for previously identified regulators such as Zelda and GAGA-factor, with multiple analyses pointing toward gene-specific regulation. The observed mechanisms of regulation are consistent with what is known about regulation in these two genomes: during oogenesis, the maternal genome is optimized to quickly produce a large volume of transcripts to provide to the oocyte; after zygotic genome activation, mechanisms are employed to activate transcription of specific genes in a spatiotemporally precise manner. Thus the genetic architecture of the maternal and zygotic genomes, and the specific requirements for the transcripts present at each stage of embryogenesis, determine the regulatory mechanisms responsible for transcripts present at these stages.
Highlights
IntroductionThe earliest stages of embryonic development are critical, as processes such as cleavage cycles and the beginnings of axial patterning become the basis for all subsequent developmental processes
Development is a sequential process, where each step builds on the one before it
To examine the regulatory basis of maternal and zygotic transcription, we surveyed the genomes of 11 Drosophila species for regulatory elements
Summary
The earliest stages of embryonic development are critical, as processes such as cleavage cycles and the beginnings of axial patterning become the basis for all subsequent developmental processes Regulation of these important tasks is controlled by mRNAs and proteins, and perhaps unsurprisingly mRNA levels in Drosophila are found to be precisely controlled during early embryogenesis [1,2]. Support cells called nurse cells synthesize RNA, proteins, and organelles which are transported into the oocyte [7] These maternally produced mRNAs are responsible for many of the critical events of early embryogenesis, such as the rapid cleavage cycles, the establishment of body axis, and the coordination of the handoff of control to the zygotic genome. This process begins with broad maternal gradients which control transcription of early zygotic gap genes, and later pair-rule genes, at precise locations within the embryo at specific developmental times [11,12]
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