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

ABSTRACT: Post-transcriptional gene regulatory mechanisms are fundamental to 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 total RNA-sequencing and quantitative mass spectrometry analysis simultaneously on Drosophila maternal-to-zygotic transition (MZT) to reveal the dynamic interchange between transcript and protein expression level at the earliest stage of animal development. 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. 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 find that stable expression of transcript can be crucial for the protein expression level upregulation during the earliest stage of MZT, and also report that proteome wide and quantitative remodeling of the distinct post translational regulatory mechanisms can be crucial for the gene expression level changes and progression of the earliest stages of animal development.

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ORGANISM(S): Drosophila Melanogaster (fruit Fly)

TISSUE(S): Embryo

SUBMITTER: Yongwoo Na

LAB HEAD: Jongeo Kim

PROVIDER: PXD057383 | Pride | 2025-09-08

REPOSITORIES: Pride

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Gene expression dynamics before and after zygotic gene activation in <i>Drosophila</i> early embryogenesis.

Na Yongwoo Y Choi Yeon Y Nguyen Thi Thanh My TTM Pham-Bui Hoang-Anh HA Kim Jeesoo J Kim V Narry VN Lee Mihye M Kim Jong-Seo JS

iScience 20250807 9

Post-transcriptional gene regulatory mechanisms are fundamental to 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 total RNA sequencing and quantitative mass spectrometry analysis simultaneously on Drosophila maternal-to-zygotic transition (MZT). Further, this study is the first to report the proteome-wide quantitative changes in protein ubiquitination in ...[more]

PMID: 40894916

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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.

Project description:The earliest stages of development in most metazoans are driven by maternally deposited proteins and mRNAs, with widespread transcriptional activation of the zygotic genome occurring hours after fertilization, at a period known as the maternal-to-zygotic transition (MZT). In Drosophila, the MZT is preceded by the transcription of a small number of genes that initiate sex determination, patterning and other essential developmental processes. The zinc-finger transcription factor Zelda (ZLD) plays a key role in the transcriptional activation of these earliest-expressed genes. To better understand the mechanisms of ZLD activation and the range of its targets, we used chromatin immunoprecipitation coupled with high-throughput sequencing (ChIP-Seq) to map regions bound by ZLD prior to (mitotic cycles 8 and 9), during (mitotic cycles 13 and early 14) and after (late mitotic cycle 14) the MZT. Although only a handful of genes are transcribed prior to mitotic cycle 10, we identified thousands of regions bound by ZLD in cycle 8-9 embryos, most of which remain bound through mitotic cycle 14. As expected, these ZLD-bound regions include the promoters and enhancers of the small subset of genes transcribed at this early stage. However we also observed ZLD bound at cycle 8-9 to the promoters of a large fraction of the several thousand genes whose first transcription does not occur until roughly an hour and four mitotic cycles later. These early ZLD-bound regions include virtually all of the thousands of known and presumed enhancers bound at cycle 14 by the transcription factors that regulate patterned gene activation during the MZT. The association between early ZLD binding and MZT activity is so strong that ZLD binding alone can be used to identify active promoters and regulatory sequences with high specificity and selectivity. This strong early association of ZLD with regions not active until the MZT suggests that ZLD is not only required for the earliest wave of transcription, but also plays a major role in activating the genome at the MZT. Genome-wide mapping of Zelda in wild-type Drosophila melanogaster embryos prior (mitotic cycles 8-9), during (cycles 13-14), and after (late cycle 14) maternal-to-zygotic transition

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Dataset Information

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

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Publications

Gene expression dynamics before and after zygotic gene activation in <i>Drosophila</i> early embryogenesis.

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Dataset Information

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

Dataset's files

Publications

Gene expression dynamics before and after zygotic gene activation in &lt;i&gt;Drosophila&lt;/i&gt; early embryogenesis.

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OmicsDI is part of the ELIXIR infrastructure

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Gene expression dynamics before and after zygotic gene activation in <i>Drosophila</i> early embryogenesis.