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Gene expression dynamics before and after zygotic genome activation in Drosophila early embryogenesis

ABSTRACT: Post-transcriptional gene regulatory mechanisms are fundamental for the determination of gene expression dynamics and especially crucial for the earliest stages of animal development in which transcription is nearly silent. Here we performed high-resolution gene expression level change analysis in Drosophila maternal-to-zygotic transition (MZT). Intriguingly, we found that both stable transcript expression and an increase in translation efficiency can be crucial for protein upregulation prior to zygotic gene activation (ZGA), whereas such features diminished following ZGA. The results suggested that there are distinct regulatory mechanisms for protein upregulation pre- and post-ZGA in Drosophila embryos. Further, this study is the first to report the proteome-wide quantitative changes in protein ubiquitination in Drosophila MZT. Our results indicate that timely ubiquitination of the distinct target proteins during MZT are essential for the downregulation of protein expression levels. Profiling of the RNA-associated proteome changes in Drosophila MZT suggested that RNA-binding activities can be regulated without the respective change in net protein expression levels for over 200 proteins, including Pcid2, Sym, and Cpsf73. Taken together, we report a diverse array of features that mediate post-transcriptionally regulated gene expression dynamics in Drosophila MZT.

ORGANISM(S): Drosophila melanogaster

PROVIDER: GSE255926 | GEO | 2025/07/17

REPOSITORIES: GEO

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Project description:Background: During the maternal-to-zygotic transition (MZT) vast changes in the embryonic transcriptome are produced by a combination of two processes: elimination of maternally provided mRNAs and synthesis of new transcripts from the zygotic genome. Previous genome-wide analyses of the MZT have been restricted to whole embryos. Here we report the first such analysis for primordial germ cells (PGCs), the progenitors of the germ-line stem cells. Results: We purified PGCs from Drosophila embryos, defined their proteome and transcriptome, and assessed the content, scale and dynamics of their MZT. Transcripts encoding proteins that implement particular types of biological functions group into nine distinct expression profiles, reflecting coordinate control at the transcriptional and posttranscriptional levels. mRNAs encoding germ-plasm components and cell-cell signaling molecules are rapidly degraded while new transcription produces mRNAs encoding the core transcriptional and protein synthetic machineries. The RNA-binding protein, Smaug, is essential for the PGC MZT, clearing transcripts encoding proteins that regulate stem cell behavior, transcriptional and posttranscriptional processes. Computational analyses suggest that Smaug and AU-rich element binding-proteins function independently to control transcript elimination. Conclusion: The scale of the MZT is similar in the soma and PGCs. However, the timing and content of their MZTs differ, reflecting the distinct developmental imperatives of these cell types. The PGC MZT is delayed relative to that in the soma, likely because relief of PGC-specific transcriptional silencing is required for zygotic genome activation as well as for efficient maternal transcript clearance. There are 26 samples in total, including 1-to-3 hour, 3-to-5 hour, 5-to-7 hour PGCs in wild type and smaug mutant flies and 1-to-3 hour somatic cells in wild type flies. Except for the 1-to-3 hour and 3-to-5 hour smaug mutant PGCs which have three replicates, all the other samples have four replicates.

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Gene expression dynamics before and after zygotic genome activation in Drosophila early embryogenesis

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