Quantifying post-transcriptional regulation in the development of Drosophila melanogaster

Becker, Kolja; Bluhm, Alina; Casas-Vila, Núria; Dinges, Nadja; Dejung, Mario; Sayols, Sergi; Kreutz, Clemens; Roignant, Jean‐Yves; Butter, Falk; Legewie, Stefan

doi:10.1038/s41467-018-07455-9

Cited by 80 publications

(88 citation statements)

References 65 publications

(92 reference statements)

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“…global transcriptome and proteome analyses prior to and during the MZT have revealed that post-translational regulation of protein stability and function also play a major role in Drosophila (Becker et al, 2018;Casas-Vila et al, 2017;Kronja et al, 2014a) and C. elegans (Stoeckius et al, 2014). For example, in C. elegans more than one-quarter of the transcriptome is downregulated at least twofold in early embryos, whereas only 5% of the proteome shows a similar decrease (Stoeckius et al, 2014).…”

Section: Post-translational Regulation Of Maternal Proteinsmentioning

confidence: 99%

The maternal-to-zygotic transition revisited

2019

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The development of animal embryos is initially directed by maternal gene products. Then, during the maternal-to-zygotic transition (MZT), developmental control is handed to the zygotic genome. Extensive research in both vertebrate and invertebrate model organisms has revealed that the MZT can be subdivided into two phases, during which very different modes of gene regulation are implemented: initially, regulation is exclusively post-transcriptional and post-translational, following which gradual activation of the zygotic genome leads to predominance of transcriptional regulation. These changes in the gene expression program of embryos are precisely controlled and highly interconnected. Here, we review current understanding of the mechanisms that underlie handover of developmental control during the MZT.

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Section: Post-translational Regulation Of Maternal Proteinsmentioning

confidence: 99%

The maternal-to-zygotic transition revisited

2019

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“…and transcriptome excluded almost all proteins in Cluster 6 from their analysis because of these 171 proteins' narrow expression window (Becker et al, 2018). 172…”

Section: Dynamics Of the Proteome Relative To The Transcriptome And Tmentioning

confidence: 99%

Precise temporal regulation of post-transcriptional repressors is required for an orderlyDrosophilamaternal-to-zygotic transition

Cao

Kabelitz

Gupta

et al. 2019

Preprint

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SUMMARYIn animal embryos the maternal-to-zygotic transition (MZT) hands developmental control from maternal to zygotic gene products. We show that the maternal proteome represents over half of the protein coding capacity of the Drosophila melanogaster 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). While the ubiquitin-proteasome system is necessary for clearance of all four 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; 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 makes the protein immune to degradation. We show that artificially persistent SMG downregulates the zygotic re-expression of mRNAs whose maternal contribution is cleared by SMG. Thus, clearance of SMG permits an orderly MZT.

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“…While this central dogma has been established over the last 60 years, the non-linearity between the levels of a given mRNA and the amount of protein it encodes has only recently started to emerge (5)(6)(7)(8). One explanation for this poor correlation resides in the spatial control of translation that could lead to differential protein output.…”

Section: Introductionmentioning

confidence: 99%

Imaging translation dynamics in live embryos reveals spatial heterogeneities

Dufourt

Bellec

Trullo

et al. 2020

Preprint

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The translation of individual mRNA molecules is a key biological process, yet this multi-step process has never been imaged in living multicellular organisms. Here we deploy the recently developed Suntag method to visualize and quantify translation dynamics of single mRNAs in living Drosophila embryos. By focusing on the translation of the conserved major epithelial-mesenchymal transition (EMT)-inducing transcription factor Twist, we identified spatial heterogeneity in mRNA translation efficiency and reveal the existence of translation factories, where clustered mRNAs are cotranslated preferentially at basal perinuclear regions. Simultaneous visualization of transcription and translation dynamics in a living multicellular organism opens exciting new avenues for understanding of gene regulation during development.

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Quantifying post-transcriptional regulation in the development of Drosophila melanogaster

Cited by 80 publications

References 65 publications

The maternal-to-zygotic transition revisited

The maternal-to-zygotic transition revisited

Precise temporal regulation of post-transcriptional repressors is required for an orderlyDrosophilamaternal-to-zygotic transition

Imaging translation dynamics in live embryos reveals spatial heterogeneities

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