Precise Temporal Regulation of Post-transcriptional Repressors Is Required for an Orderly Drosophila Maternal-to-Zygotic Transition

Wen Xi Cao, Sarah Kabelitz, Meera Gupta, Eyan Yeung, Sichun Lin, Christiane Rammelt, Christian Ihling, Filip Pekovic, Timothy C.H. Low, Najeeb U. Siddiqui, Matthew H.K. Cheng, Stephane Angers, Craig A. Smibert, Martin Wühr, Elmar Wahle, Howard D. Lipshitz

Research output: Contribution to journalArticle

Abstract

In animal embryos, the maternal-to-zygotic transition (MZT) hands developmental control from maternal to zygotic gene products. We show that the maternal proteome represents more than half of the protein-coding capacity of Drosophila melanogaster's genome, and that 2% of this proteome is rapidly degraded during the MZT. Cleared proteins include the post-transcriptional repressors Cup, Trailer hitch (TRAL), Maternal expression at 31B (ME31B), and Smaug (SMG). Although the ubiquitin-proteasome system is necessary for clearance of these repressors, distinct E3 ligase complexes target them: the C-terminal to Lis1 Homology (CTLH) complex targets Cup, TRAL, and ME31B for degradation early in the MZT and the Skp/Cullin/F-box-containing (SCF) complex targets SMG at the end of the MZT. Deleting the C-terminal 233 amino acids of SMG abrogates F-box protein interaction and confers immunity to degradation. Persistent SMG downregulates zygotic re-expression of mRNAs whose maternal contribution is degraded by SMG. Thus, clearance of SMG permits an orderly MZT.

Original languageEnglish (US)
Article number107783
JournalCell Reports
Volume31
Issue number12
DOIs
StatePublished - Jun 23 2020

All Science Journal Classification (ASJC) codes

  • Biochemistry, Genetics and Molecular Biology(all)

Keywords

  • Cup
  • embryogenesis
  • ME31B
  • proteome
  • RNA-binding
  • Smaug
  • Trailer hitch
  • ubiquitin ligase

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  • Cite this

    Cao, W. X., Kabelitz, S., Gupta, M., Yeung, E., Lin, S., Rammelt, C., Ihling, C., Pekovic, F., Low, T. C. H., Siddiqui, N. U., Cheng, M. H. K., Angers, S., Smibert, C. A., Wühr, M., Wahle, E., & Lipshitz, H. D. (2020). Precise Temporal Regulation of Post-transcriptional Repressors Is Required for an Orderly Drosophila Maternal-to-Zygotic Transition. Cell Reports, 31(12), [107783]. https://doi.org/10.1016/j.celrep.2020.107783