Dynamic patterning by the Drosophila pair-rule network reconciles long-germ and short-germ segmentation

PLoS Biol. 2017 Sep 27;15(9):e2002439. doi: 10.1371/journal.pbio.2002439. eCollection 2017 Sep.

Abstract

Drosophila segmentation is a well-established paradigm for developmental pattern formation. However, the later stages of segment patterning, regulated by the "pair-rule" genes, are still not well understood at the system level. Building on established genetic interactions, I construct a logical model of the Drosophila pair-rule system that takes into account the demonstrated stage-specific architecture of the pair-rule gene network. Simulation of this model can accurately recapitulate the observed spatiotemporal expression of the pair-rule genes, but only when the system is provided with dynamic "gap" inputs. This result suggests that dynamic shifts of pair-rule stripes are essential for segment patterning in the trunk and provides a functional role for observed posterior-to-anterior gap domain shifts that occur during cellularisation. The model also suggests revised patterning mechanisms for the parasegment boundaries and explains the aetiology of the even-skipped null mutant phenotype. Strikingly, a slightly modified version of the model is able to pattern segments in either simultaneous or sequential modes, depending only on initial conditions. This suggests that fundamentally similar mechanisms may underlie segmentation in short-germ and long-germ arthropods.

MeSH terms

  • Animals
  • Body Patterning / genetics*
  • Computer Simulation
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / embryology*
  • Drosophila melanogaster / genetics*
  • Embryo, Nonmammalian / metabolism
  • Embryonic Development / genetics*
  • Gene Expression Regulation, Developmental
  • Gene Regulatory Networks*
  • Models, Genetic*
  • Mutation / genetics
  • Phenotype
  • Time Factors

Substances

  • Drosophila Proteins

Grant support

Isaac Newton Trust www.newtontrust.cam.ac.uk. Research grant. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Biotechnology and Biological Sciences Research Council www.bbsrc.ac.uk. Genes to Organisms PhD studentship. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.