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Upregulation of Forces and Morphogenic Asymmetries in Dorsal Closure during Drosophila Development

X. G. Peralta ^*, Y. Toyama ^*, M. S. Hutson , R. Montague , S. Venakides , D. P. Kiehart  and G. S. Edwards ^*

Departments of ^* Physics, Biology, and Mathematics, Duke University, Durham, North Carolina; and Department of Physics and Astronomy, Vanderbilt University, Nashville, Tennessee

Correspondence: Address reprint requests to D. P. Kiehart, E-mail: dkiehart{at}duke.edu.

Tissue dynamics during dorsal closure, a stage of Drosophila development, provide a model system for cell sheet morphogenesis and wound healing. Dorsal closure is characterized by complex cell sheet movements, driven by multiple tissue specific forces, which are coordinated in space, synchronized in time, and resilient to UV-laser perturbations. The mechanisms responsible for these attributes are not fully understood. We measured spatial, kinematic, and dynamic antero-posterior asymmetries to biophysically characterize both resiliency to laser perturbations and failure of closure in mutant embryos and compared them to natural asymmetries in unperturbed, wild-type closure. We quantified and mathematically modeled two processes that are upregulated to provide resiliency—contractility of the amnioserosa and formation of a seam between advancing epidermal sheets, i.e., zipping. Both processes are spatially removed from the laser-targeted site, indicating they are not a local response to laser-induced wounding and suggesting mechanosensitive and/or chemosensitive mechanisms for upregulation. In mutant embryos, tissue junctions initially fail at the anterior end indicating inhomogeneous mechanical stresses attributable to head involution, another developmental process that occurs concomitant with the end stages of closure. Asymmetries in these mutants are reversed compared to wild-type, and inhomogeneous stresses may cause asymmetries in wild-type closure.

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