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

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  • dc.contributor.author Verd Fernández, Berta, 1984-
  • dc.contributor.author Clark, Erik
  • dc.contributor.author Wotton, Karl R.
  • dc.contributor.author Janssens, Hilde
  • dc.contributor.author Jiménez Guri, Eva
  • dc.contributor.author Crombach, Anton
  • dc.contributor.author Jaeger, Johannes, 1973-
  • dc.date.accessioned 2019-12-03T07:57:48Z
  • dc.date.available 2019-12-03T07:57:48Z
  • dc.date.issued 2018
  • dc.description.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.
  • dc.description.sponsorship 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.
  • dc.format.mimetype application/pdf
  • dc.identifier.citation Verd B, Clark E, Wotton KR, Janssens H, Jiménez-Guri E, Crombach A et al. A damped oscillator imposes temporal order on posterior gap gene expression in Drosophila. PLoS Biol. 2018;16(2):e2003174. DOI: 10.1371/journal.pbio.2003174
  • dc.identifier.doi http://dx.doi.org/10.1371/journal.pbio.2003174
  • dc.identifier.issn 1544-9173
  • dc.identifier.uri http://hdl.handle.net/10230/43058
  • dc.language.iso eng
  • dc.publisher Public Library of Science (PLoS)
  • dc.relation.ispartof PLOS Biology. 2018;16(2):e2003174
  • dc.relation.projectID info:eu-repo/grantAgreement/EC/FP7/289434
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/3PN/BFU2009-10184
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/3PN/BFU2012-33775
  • dc.relation.projectID info:eu-repo/grantAgreement/ES/3PN/SEV-2012-0208
  • dc.rights © 2018 Verd et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
  • dc.rights.accessRights info:eu-repo/semantics/openAccess
  • dc.rights.uri http://creativecommons.org/licenses/by/4.0/
  • dc.subject.keyword Gene expression
  • dc.subject.keyword Embryos
  • dc.subject.keyword Genetic oscillators
  • dc.subject.keyword Gene regulation
  • dc.subject.keyword Drosophila melanogaster
  • dc.subject.keyword Morphogenic segmentation
  • dc.subject.keyword Blastoderm
  • dc.subject.keyword Dynamical systems
  • dc.title A damped oscillator imposes temporal order on posterior gap gene expression in Drosophila
  • dc.type info:eu-repo/semantics/article
  • dc.type.version info:eu-repo/semantics/publishedVersion

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