A timer gene network is spatially regulated by the terminal system in the Drosophila embryo

  1. Erik Clark  Is a corresponding author
  2. Margherita Battistara
  3. Matthew Alan Benton  Is a corresponding author
  1. University of Cambridge, United Kingdom

Abstract

In insect embryos, anteroposterior patterning is coordinated by the sequential expression of the 'timer' genes caudal, Dichaete and odd-paired, whose expression dynamics correlate with the mode of segmentation. In Drosophila, the timer genes are expressed broadly across much of the blastoderm, which segments simultaneously, but their expression is delayed in a small 'tail' region, just anterior to the hindgut, which segments during germband extension. Specification of the tail and the hindgut depends on the terminal gap gene tailless, but beyond this the regulation of the timer genes is poorly understood. We used a combination of multiplexed imaging, mutant analysis, and gene network modelling to resolve the regulation of the timer genes, identifying 11 new regulatory interactions and clarifying the mechanism of posterior terminal patterning. We propose that a dynamic Tailless expression gradient modulates the intrinsic dynamics of a timer gene cross-regulatorymodule, delineating the tail region and delaying its developmental maturation.

Data availability

All necessary data are included in the main text, appendices, and supplementary information. The confocal imaging dataset on which this study is based is freely available to download from the BioImage Archive (http://www.ebi.ac.uk/bioimage-archive) under accession number S-BIAD582. This 335 GB dataset contains multiplexed image stacks of more than 800 individual embryos, including 12 different genotypes and over 50 different genotype / gene product combinations. Image analysis code is provided Appendix 2-Figure 1-source data 1. A list of the corresponding image file(s) within the dataset for all figure panels within the main text, appendices, and supplementary information is provided in Appendix 2-Figure 1-source data 2. Source Data files are provided for the expression traces in the main and supplementary figures.

The following data sets were generated

Article and author information

Author details

  1. Erik Clark

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    ec491@cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5588-796X
  2. Margherita Battistara

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Matthew Alan Benton

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    matthewabenton@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7953-0765

Funding

Biotechnology and Biological Sciences Research Council (Research Grant BB/P009336/1)

  • Erik Clark

Trinity College, University of Cambridge (Junior Research Fellowship)

  • Erik Clark

European Molecular Biology Organization (Postodoctoral Fellowship ALTF 383-2018)

  • Erik Clark

Deutsche Forschungsgemeinschaft (Research Fellowship BE 6732/1-1)

  • Matthew Alan Benton

Isaac Newton Trust (Research Grant)

  • Matthew Alan Benton

Department of Zoology, University of Cambridge

  • Matthew Alan Benton

Wellcome Trust (PhD Studentship)

  • Margherita Battistara

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Gáspár Jékely, University of Exeter, United Kingdom

Publication history

  1. Received: March 23, 2022
  2. Accepted: December 15, 2022
  3. Accepted Manuscript published: December 16, 2022 (version 1)

Copyright

© 2022, Clark et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Erik Clark
  2. Margherita Battistara
  3. Matthew Alan Benton
(2022)
A timer gene network is spatially regulated by the terminal system in the Drosophila embryo
eLife 11:e78902.
https://doi.org/10.7554/eLife.78902

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