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A damped oscillator imposes temporal order on posterior gap gene expression in Drosophila

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  • Berta Verd
  • Erik Clark
  • Karl R Wotton
  • Hilde Janssens
  • Eva Jiménez-Guri
  • Anton Crombach
  • Johannes Jaeger

Abstract

Insects determine their body segments in two different ways. Short-germband insects, such as the flour beetle Tribolium castaneum, use a molecular clock to establish segments sequentially. In contrast, long-germband insects, such as the vinegar fly Drosophila melanogaster, determine all segments simultaneously through a hierarchical cascade of gene regulation. Gap genes constitute the first layer of the Drosophila segmentation gene hierarchy, downstream of maternal gradients such as that of Caudal (Cad). We use data-driven mathematical modelling and phase space analysis to show that shifting gap domains in the posterior half of the Drosophila embryo are an emergent property of a robust damped oscillator mechanism, suggesting that the regulatory dynamics underlying long- and short-germband segmentation are much more similar than previously thought. In Tribolium, Cad has been proposed to modulate the frequency of the segmentation oscillator. Surprisingly, our simulations and experiments show that the shift rate of posterior gap domains is independent of maternal Cad levels in Drosophila. Our results suggest a novel evolutionary scenario for the short- to long-germband transition and help explain why this transition occurred convergently multiple times during the radiation of the holometabolan insects.Author summary: Different insect species exhibit one of two distinct modes of determining their body segments (known as segmentation) during development: they either use a molecular oscillator to position segments sequentially, or they generate segments simultaneously through a hierarchical gene-regulatory cascade. The sequential mode is ancestral, while the simultaneous mode has been derived from it independently several times during evolution. In this paper, we present evidence suggesting that simultaneous segmentation also involves an oscillator in the posterior end of the embryo of the vinegar fly, Drosophila melanogaster. This surprising result indicates that both modes of segment determination are much more similar than previously thought. Such similarity provides an important step towards our understanding of the frequent evolutionary transitions observed between sequential and simultaneous segmentation.

Suggested Citation

  • Berta Verd & Erik Clark & Karl R Wotton & Hilde Janssens & Eva Jiménez-Guri & Anton Crombach & Johannes Jaeger, 2018. "A damped oscillator imposes temporal order on posterior gap gene expression in Drosophila," PLOS Biology, Public Library of Science, vol. 16(2), pages 1-24, February.
  • Handle: RePEc:plo:pbio00:2003174
    DOI: 10.1371/journal.pbio.2003174
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    References listed on IDEAS

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    1. Maksat Ashyraliyev & Ken Siggens & Hilde Janssens & Joke Blom & Michael Akam & Johannes Jaeger, 2009. "Gene Circuit Analysis of the Terminal Gap Gene huckebein," PLOS Computational Biology, Public Library of Science, vol. 5(10), pages 1-16, October.
    2. Manu & Svetlana Surkova & Alexander V Spirov & Vitaly V Gursky & Hilde Janssens & Ah-Ram Kim & Ovidiu Radulescu & Carlos E Vanario-Alonso & David H Sharp & Maria Samsonova & John Reinitz, 2009. "Canalization of Gene Expression and Domain Shifts in the Drosophila Blastoderm by Dynamical Attractors," PLOS Computational Biology, Public Library of Science, vol. 5(3), pages 1-15, March.
    3. François Giudicelli & Ertuğrul M Özbudak & Gavin J Wright & Julian Lewis, 2007. "Setting the Tempo in Development: An Investigation of the Zebrafish Somite Clock Mechanism," PLOS Biology, Public Library of Science, vol. 5(6), pages 1-15, May.
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