Abstract

The maternal-to-zygotic transition (MZT) is a conserved step in animal development, where control is passed from the maternal to the zygotic genome. Although the MZT is typically considered from its impact on the transcriptome, we previously found that three maternally deposited Drosophila RNA-binding proteins (ME31B, Trailer Hitch [TRAL], and Cup) are also cleared during the MZT by unknown mechanisms. Here, we show that these proteins are degraded by the ubiquitin-proteasome system. Marie Kondo, an E2 conjugating enzyme, and the E3 CTLH ligase are required for the destruction of ME31B, TRAL, and Cup. Structure modeling of the Drosophila CTLH complex suggests that substrate recognition is different than orthologous complexes. Despite occurring hours earlier, egg activation mediates clearance of these proteins through the Pan Gu kinase, which stimulates translation of Kdo mRNA. Clearance of the maternal protein dowry thus appears to be a coordinated, but as-yet underappreciated, aspect of the MZT.

Highlights

  • Proper embryogenesis is critical for animal development

  • Note that less heterogeneity in fluorescence was observed in the mutant embryos; this observation likely stems from the fact that in wild-type embryos some ME31B-GFP degradation occurs during embryo collection and staging, but almost none occurs in png50 embryos

  • Through a medium-scale RNAi screen, we identified that the E2 conjugating enzyme Kdo is required for the clearance of ME31B, TRAL, and Cup (Figure 3)

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Summary

Introduction

Many of the earliest events occur prior to the onset of zygotic transcription, and they are instead directed by maternally deposited proteins and messenger RNAs (mRNAs). We found that three RNA-binding proteins (ME31B, Trailer Hitch [TRAL], and Cup) are rapidly degraded during the MZT in Drosophila melanogaster, at a time point coinciding with the major wave of zygotic transcription (Wang et al, 2017). All three proteins are required for oogenesis, and they appear to bind and repress thousands of deposited maternal mRNAs (Keyes and Spradling, 1997; Nakamura et al, 2001; Tritschler et al, 2008; Wang et al, 2017; Wilhelm et al, 2003).

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