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The segment polarity network is a robust developmental module

Author

Listed:
  • George von Dassow

    (University of Washington, Box 351800)

  • Eli Meir

    (University of Washington, Box 351800)

  • Edwin M. Munro

    (University of Washington, Box 351800)

  • Garrett M. Odell

    (University of Washington, Box 351800)

Abstract

All insects possess homologous segments, but segment specification differs radically among insect orders. In Drosophila, maternal morphogens control the patterned activation of gap genes, which encode transcriptional regulators that shape the patterned expression of pair-rule genes. This patterning cascade takes place before cellularization. Pair-rule gene products subsequently ‘imprint’ segment polarity genes with reiterated patterns, thus defining the primordial segments. This mechanism must be greatly modified in insect groups in which many segments emerge only after cellularization1. In beetles and parasitic wasps, for instance, pair-rule homologues are expressed in patterns consistent with roles during segmentation, but these patterns emerge within cellular fields2,3,4. In contrast, although in locusts pair-rule homologues may not control segmentation5,6, some segment polarity genes and their interactions are conserved3,7,8,9,10. Perhaps segmentation is modular, with each module autonomously expressing a characteristic intrinsic behaviour in response to transient stimuli. If so, evolution could rearrange inputs to modules without changing their intrinsic behaviours. Here we suggest, using computer simulations, that the Drosophila segment polarity genes constitute such a module, and that this module is resistant to variations in the kinetic constants that govern its behaviour.

Suggested Citation

  • George von Dassow & Eli Meir & Edwin M. Munro & Garrett M. Odell, 2000. "The segment polarity network is a robust developmental module," Nature, Nature, vol. 406(6792), pages 188-192, July.
    • Handle: RePEc:nat:nature:v:406:y:2000:i:6792:d:10.1038_35018085
    DOI: 10.1038/35018085
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    Cited by:

    1. Stefano Ciliberti & Olivier C Martin & Andreas Wagner, 2007. "Robustness Can Evolve Gradually in Complex Regulatory Gene Networks with Varying Topology," PLOS Computational Biology, Public Library of Science, vol. 3(2), pages 1-10, February.
    2. Manuel Cambón & Óscar Sánchez, 2022. "Thermodynamic Modelling of Transcriptional Control: A Sensitivity Analysis," Mathematics, MDPI, vol. 10(13), pages 1-18, June.
    3. Zeina Shreif & Vipul Periwal, 2014. "A Network Characteristic That Correlates Environmental and Genetic Robustness," PLOS Computational Biology, Public Library of Science, vol. 10(2), pages 1-23, February.
    4. Carl Song & Hilary Phenix & Vida Abedi & Matthew Scott & Brian P Ingalls & Mads Kærn & Theodore J Perkins, 2010. "Estimating the Stochastic Bifurcation Structure of Cellular Networks," PLOS Computational Biology, Public Library of Science, vol. 6(3), pages 1-11, March.
    5. Adel Dayarian & Madalena Chaves & Eduardo D Sontag & Anirvan M Sengupta, 2009. "Shape, Size, and Robustness: Feasible Regions in the Parameter Space of Biochemical Networks," PLOS Computational Biology, Public Library of Science, vol. 5(1), pages 1-12, January.
    6. Guillermo Rodrigo & Santiago F Elena, 2011. "Structural Discrimination of Robustness in Transcriptional Feedforward Loops for Pattern Formation," PLOS ONE, Public Library of Science, vol. 6(2), pages 1-7, February.
    7. Miles Miller & Marc Hafner & Eduardo Sontag & Noah Davidsohn & Sairam Subramanian & Priscilla E M Purnick & Douglas Lauffenburger & Ron Weiss, 2012. "Modular Design of Artificial Tissue Homeostasis: Robust Control through Synthetic Cellular Heterogeneity," PLOS Computational Biology, Public Library of Science, vol. 8(7), pages 1-18, July.
    8. Ryan N Gutenkunst & Joshua J Waterfall & Fergal P Casey & Kevin S Brown & Christopher R Myers & James P Sethna, 2007. "Universally Sloppy Parameter Sensitivities in Systems Biology Models," PLOS Computational Biology, Public Library of Science, vol. 3(10), pages 1-8, October.
    9. Debasish Mondal & Edward Dougherty & Abhishek Mukhopadhyay & Adria Carbo & Guang Yao & Jianhua Xing, 2014. "Systematic Reverse Engineering of Network Topologies: A Case Study of Resettable Bistable Cellular Responses," PLOS ONE, Public Library of Science, vol. 9(8), pages 1-12, August.
    10. Merav Socolovsky & Michael Murrell & Ying Liu & Ramona Pop & Ermelinda Porpiglia & Andre Levchenko, 2007. "Negative Autoregulation by FAS Mediates Robust Fetal Erythropoiesis," PLOS Biology, Public Library of Science, vol. 5(10), pages 1-16, September.
    11. Cummings, F.W, 2004. "A model of morphogenesis," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 339(3), pages 531-547.
    12. Andreas Wagner, 2015. "Causal Drift, Robust Signaling, and Complex Disease," PLOS ONE, Public Library of Science, vol. 10(3), pages 1-29, March.

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