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Dynamic control of positional information in the early Drosophila embryo

Author

Listed:
  • Johannes Jaeger

    (Stony Brook University)

  • Svetlana Surkova

    (St Petersburg State Polytechnic University)

  • Maxim Blagov

    (St Petersburg State Polytechnic University)

  • Hilde Janssens

    (Stony Brook University)

  • David Kosman

    (University of California)

  • Konstantin N. Kozlov

    (St Petersburg State Polytechnic University)

  • Manu

    (Stony Brook University)

  • Ekaterina Myasnikova

    (St Petersburg State Polytechnic University)

  • Carlos E. Vanario-Alonso

    (Stony Brook University
    Universidade Federal do Rio de Janeiro, Instituto de Biofísica Carlos Chagas Filho, Rio de Janeiro)

  • Maria Samsonova

    (St Petersburg State Polytechnic University)

  • David H. Sharp

    (Los Alamos National Laboratory)

  • John Reinitz

    (Stony Brook University)

Abstract

Morphogen gradients contribute to pattern formation by determining positional information in morphogenetic fields1,2. Interpretation of positional information is thought to rely on direct, concentration-threshold-dependent mechanisms for establishing multiple differential domains of target gene expression1,3,4. In Drosophila, maternal gradients establish the initial position of boundaries for zygotic gap gene expression, which in turn convey positional information to pair-rule and segment-polarity genes, the latter forming a segmental pre-pattern by the onset of gastrulation5,6,7. Here we report, on the basis of quantitative gene expression data, substantial anterior shifts in the position of gap domains after their initial establishment. Using a data-driven mathematical modelling approach8,9,10,11, we show that these shifts are based on a regulatory mechanism that relies on asymmetric gap–gap cross-repression and does not require the diffusion of gap proteins. Our analysis implies that the threshold-dependent interpretation of maternal morphogen concentration is not sufficient to determine shifting gap domain boundary positions, and suggests that establishing and interpreting positional information are not independent processes in the Drosophila blastoderm.

Suggested Citation

  • Johannes Jaeger & Svetlana Surkova & Maxim Blagov & Hilde Janssens & David Kosman & Konstantin N. Kozlov & Manu & Ekaterina Myasnikova & Carlos E. Vanario-Alonso & Maria Samsonova & David H. Sharp & J, 2004. "Dynamic control of positional information in the early Drosophila embryo," Nature, Nature, vol. 430(6997), pages 368-371, July.
  • Handle: RePEc:nat:nature:v:430:y:2004:i:6997:d:10.1038_nature02678
    DOI: 10.1038/nature02678
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    Citations

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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. Kolja Becker & Eva Balsa-Canto & Damjan Cicin-Sain & Astrid Hoermann & Hilde Janssens & Julio R Banga & Johannes Jaeger, 2013. "Reverse-Engineering Post-Transcriptional Regulation of Gap Genes in Drosophila melanogaster," PLOS Computational Biology, Public Library of Science, vol. 9(10), pages 1-16, October.
    3. David M Holloway & Alexander V Spirov, 2017. "Transcriptional bursting in Drosophila development: Stochastic dynamics of eve stripe 2 expression," PLOS ONE, Public Library of Science, vol. 12(4), pages 1-24, April.
    4. Theodore J Perkins & Johannes Jaeger & John Reinitz & Leon Glass, 2006. "Reverse Engineering the Gap Gene Network of Drosophila melanogaster," PLOS Computational Biology, Public Library of Science, vol. 2(5), pages 1-12, May.
    5. Bernd Boehm & Henrik Westerberg & Gaja Lesnicar-Pucko & Sahdia Raja & Michael Rautschka & James Cotterell & Jim Swoger & James Sharpe, 2010. "The Role of Spatially Controlled Cell Proliferation in Limb Bud Morphogenesis," PLOS Biology, Public Library of Science, vol. 8(7), pages 1-21, July.
    6. Ronald Thenius & Michael Bodi & Thomas Schmickl & Karl Crailsheim, 2013. "Novel method of virtual embryogenesis for structuring Artificial Neural Network controllers," Mathematical and Computer Modelling of Dynamical Systems, Taylor & Francis Journals, vol. 19(4), pages 375-387.
    7. Stradner, Jürgen & Thenius, Ronald & Zahadat, Payam & Hamann, Heiko & Crailsheim, Karl & Schmickl, Thomas, 2013. "Algorithmic requirements for swarm intelligence in differently coupled collective systems," Chaos, Solitons & Fractals, Elsevier, vol. 50(C), pages 100-114.
    8. 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.
    9. 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.
    10. 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.

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