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Precision of Readout at the hunchback Gene: Analyzing Short Transcription Time Traces in Living Fly Embryos

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  • Jonathan Desponds
  • Huy Tran
  • Teresa Ferraro
  • Tanguy Lucas
  • Carmina Perez Romero
  • Aurelien Guillou
  • Cecile Fradin
  • Mathieu Coppey
  • Nathalie Dostatni
  • Aleksandra M Walczak

Abstract

The simultaneous expression of the hunchback gene in the numerous nuclei of the developing fly embryo gives us a unique opportunity to study how transcription is regulated in living organisms. A recently developed MS2-MCP technique for imaging nascent messenger RNA in living Drosophila embryos allows us to quantify the dynamics of the developmental transcription process. The initial measurement of the morphogens by the hunchback promoter takes place during very short cell cycles, not only giving each nucleus little time for a precise readout, but also resulting in short time traces of transcription. Additionally, the relationship between the measured signal and the promoter state depends on the molecular design of the reporting probe. We develop an analysis approach based on tailor made autocorrelation functions that overcomes the short trace problems and quantifies the dynamics of transcription initiation. Based on live imaging data, we identify signatures of bursty transcription initiation from the hunchback promoter. We show that the precision of the expression of the hunchback gene to measure its position along the anterior-posterior axis is low both at the boundary and in the anterior even at cycle 13, suggesting additional post-transcriptional averaging mechanisms to provide the precision observed in fixed embryos.Author Summary: The fly embryo provides a natural laboratory to study the dynamics of transcription and its implications for the developing organism. Using live imaging experiments we investigate the nature of transcription regulation of the hunchback gene—the first to read out the maternal Bicoid gradient. While traditional time trace analysis methods based on OFF time distributions or autocorrelation functions fail for short signals, our tailored autocorrelation function overcomes these limitations revealing bursty dynamics that is reproducible between cell cycles and embryos. The inferred rates result in a lot of variability in the readout of nuclei sensing similar Bicoid concentrations, suggesting additional readout mechanisms than a one-to-one mapping of the input onto the output.

Suggested Citation

  • Jonathan Desponds & Huy Tran & Teresa Ferraro & Tanguy Lucas & Carmina Perez Romero & Aurelien Guillou & Cecile Fradin & Mathieu Coppey & Nathalie Dostatni & Aleksandra M Walczak, 2016. "Precision of Readout at the hunchback Gene: Analyzing Short Transcription Time Traces in Living Fly Embryos," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-31, December.
  • Handle: RePEc:plo:pcbi00:1005256
    DOI: 10.1371/journal.pcbi.1005256
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    References listed on IDEAS

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    1. Yihan Lin & Chang Ho Sohn & Chiraj K. Dalal & Long Cai & Michael B. Elowitz, 2015. "Combinatorial gene regulation by modulation of relative pulse timing," Nature, Nature, vol. 527(7576), pages 54-58, November.
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    Cited by:

    1. Jonathan Liu & Donald Hansen & Elizabeth Eck & Yang Joon Kim & Meghan Turner & Simon Alamos & Hernan Garcia, 2021. "Real-time single-cell characterization of the eukaryotic transcription cycle reveals correlations between RNA initiation, elongation, and cleavage," PLOS Computational Biology, Public Library of Science, vol. 17(5), pages 1-26, May.
    2. Jiaxi Zhao & Nicholas C. Lammers & Simon Alamos & Yang Joon Kim & Gabriella Martini & Hernan G. Garcia, 2024. "Optogenetic dissection of transcriptional repression in a multicellular organism," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

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