A damped oscillator imposes temporal order on posterior gap gene expression in Drosophila.
Wotton, Karl R
Public Library of Science (PLoS)
MetadataShow full item record
Verd, B., Clark, E., Wotton, K. R., Janssens, H., Jiménez-Guri, E., Crombach, A., & Jaeger, J. (2018). A damped oscillator imposes temporal order on posterior gap gene expression in Drosophila.. PLoS biology, 16 (2), e2003174. https://doi.org/10.1371/journal.pbio.2003174
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.
Animals, Tribolium, Drosophila melanogaster, Drosophila Proteins, Species Specificity, Gene Expression Regulation, Developmental, Biological Clocks, Body Patterning, Time Factors, Gene Regulatory Networks
MINECO BFU2009-10184/BFU2012-33775/SEV-2012-0208 European Commission FP7/KBBE-2011/5/289434 La Caixa Savings Bank (PhD fellowship to BV) KLI Klosterneuburg (PhD Writing-up & Postdoctoral Fellowships to BV) Wissenschaftskolleg zu Berlin (Wiko) (Fellowships to JJ and AC)
External DOI: https://doi.org/10.1371/journal.pbio.2003174
This record's URL: https://www.repository.cam.ac.uk/handle/1810/279450
Attribution 4.0 International (CC BY 4.0)
Licence URL: https://creativecommons.org/licenses/by/4.0/