IDEAS home Printed from https://ideas.repec.org/a/plo/pbio00/2002439.html
   My bibliography  Save this article

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

Author

Listed:
  • Erik Clark

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.Author summary: Segmentation in insects involves the division of the body into several repetitive units. In Drosophila embryos, all segments are patterned rapidly and simultaneously during early development, in a process known as “long-germ” embryogenesis. In contrast, many insect embryos retain an ancestral or “short-germ” mode of development, in which segments are patterned sequentially, from head to tail, over a period of time. In both types of embryo, the patterning of segment boundaries is regulated by a network of so-called “pair-rule” genes. These networks are thought to be quite divergent due to the different expression patterns observed for the pair-rule genes in each case: regularly spaced arrays of transient stripes in Drosophila, and dynamic expression within a posterior “segment addition zone” in short-germ insects. However, even in Drosophila, a clear understanding of pair-rule patterning has been lacking. Here, I make a computational model of the Drosophila pair-rule network and use simulations to explore how segmentation works. Surprisingly, I find that Drosophila segment patterning relies on pair-rule gene expression moving across cells over time. This conclusion differs from older models of pair-rule patterning but is consistent with the subtly dynamic nature of pair-rule stripes in real embryos, previously described in quantitative studies. I conclude that long-germ and short-germ segmentation involve similar expression dynamics at the level of individual cells, even though they look very different at the level of whole tissues. This suggests that the gene networks involved may be much more conserved than previously thought.

Suggested Citation

  • Erik Clark, 2017. "Dynamic patterning by the Drosophila pair-rule network reconciles long-germ and short-germ segmentation," PLOS Biology, Public Library of Science, vol. 15(9), pages 1-38, September.
  • Handle: RePEc:plo:pbio00:2002439
    DOI: 10.1371/journal.pbio.2002439
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.2002439
    Download Restriction: no

    File URL: https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.2002439&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pbio.2002439?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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 in the Drosophila Blastoderm by Gap Gene Cross Regulation," PLOS Biology, Public Library of Science, vol. 7(3), pages 1-13, March.
    2. Jonathan Desponds & Huy Tran & Teresa Ferraro & Tanguy Lucas & Carmina Perez Romero & Aurelien Guillou & Cecile Fradin & Mathieu Coppey & Nathalie Dostatni & Aleksandra M Walczak, 2016. "Precision of Readout at the hunchback Gene: Analyzing Short Transcription Time Traces in Living Fly Embryos," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-31, December.
    3. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Yurie Okabe-Oho & Hiroki Murakami & Suguru Oho & Masaki Sasai, 2009. "Stable, Precise, and Reproducible Patterning of Bicoid and Hunchback Molecules in the Early Drosophila Embryo," PLOS Computational Biology, Public Library of Science, vol. 5(8), pages 1-20, August.
    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. Jiaxi Zhao & Nicholas C. Lammers & Simon Alamos & Yang Joon Kim & Gabriella Martini & Hernan G. Garcia, 2024. "Optogenetic dissection of transcriptional repression in a multicellular organism," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    4. 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.
    5. Ruben Perez-Carrasco & Pilar Guerrero & James Briscoe & Karen M Page, 2016. "Intrinsic Noise Profoundly Alters the Dynamics and Steady State of Morphogen-Controlled Bistable Genetic Switches," PLOS Computational Biology, Public Library of Science, vol. 12(10), pages 1-23, October.
    6. Jonathan Liu & Donald Hansen & Elizabeth Eck & Yang Joon Kim & Meghan Turner & Simon Alamos & Hernan Garcia, 2021. "Real-time single-cell characterization of the eukaryotic transcription cycle reveals correlations between RNA initiation, elongation, and cleavage," PLOS Computational Biology, Public Library of Science, vol. 17(5), pages 1-26, May.
    7. 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.
    8. Berta Verd & Anton Crombach & Johannes Jaeger, 2017. "Dynamic Maternal Gradients Control Timing and Shift-Rates for Drosophila Gap Gene Expression," PLOS Computational Biology, Public Library of Science, vol. 13(2), pages 1-23, February.
    9. 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 in the Drosophila Blastoderm by Gap Gene Cross Regulation," PLOS Biology, Public Library of Science, vol. 7(3), pages 1-13, March.
    10. Diego Calzolari & Giovanni Paternostro & Patrick L Harrington Jr. & Carlo Piermarocchi & Phillip M Duxbury, 2007. "Selective Control of the Apoptosis Signaling Network in Heterogeneous Cell Populations," PLOS ONE, Public Library of Science, vol. 2(6), pages 1-12, June.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pbio00:2002439. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosbiology (email available below). General contact details of provider: https://journals.plos.org/plosbiology/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.