Abstract
SummaryDuring development, cell-generated forces induce tissue-scale deformations to shape the organism [1, 2]. The pattern and extent of these deformations depend not solely on the temporal and spatial profile of the generated force fields but also on the mechanical properties of the tissues that the forces act on. It is thus conceivable that, much like the cell-generated forces, the mechanical properties of tissues are modulated during development in order to drive morphogenesis toward specific developmental endpoints. Although many approaches have recently emerged to assess effective mechanical parameters of tissues [3, 4, 5, 6, 7, 8], they could not quantitatively relate spatially localized force induction to tissue-scale deformations in vivo. Here, we present a method that overcomes this limitation. Our approach is based on the application of controlled forces on a single microparticle embedded in an individual cell of an embryo. Combining measurements of bead displacement with the analysis of induced deformation fields in a continuum mechanics framework, we quantify material properties of the tissue and follow their changes over time. In particular, we uncover a rapid change in tissue response occurring during Drosophila cellularization, resulting from a softening of the blastoderm and an increase of external friction. We find that the microtubule cytoskeleton is a major contributor to epithelial mechanics at this stage. We identify developmentally controlled modulations in perivitelline spacing that can account for the changes in friction. Overall, our method allows for the measurement of key mechanical parameters governing tissue-scale deformations and flows occurring during morphogenesis.
Highlights
Applying forces at consecutive intervals in the blastoderm, spanning a period of 50 min before gastrulation in Resille-GFPexpressing embryos, we observe significant changes in both the displacement of the bead and the induced deformation field (Figures 1B and 1C; Video S2)
To probe epithelial mechanics at early developmental stages, we have developed a protocol for injecting an individual magnetic microparticle into a single cell within a specific tissue of a living Drosophila embryo (Figures 1A, 1B, and S1G; Video S1; STAR Methods)
We obtained two complementary readouts characterizing the mechanical response of the tissue: (1) the bead displacement over time, and (2) the deformation field of the apical surface area of the epithelium (Figures 1B and 1C; STAR Methods)
Summary
Applying forces at consecutive intervals in the blastoderm, spanning a period of 50 min before gastrulation in Resille-GFPexpressing embryos, we observe significant changes in both the displacement of the bead and the induced deformation field (Figures 1B and 1C; Video S2). Defining the origin of time as the onset of gastrulation, we find that the amplitude of bead displacement, i.e., the maximal displacement of the bead at the end of the force step relative to its position before the force step, changes abruptly from approximately 2 mm to 8 mm at around t = À16 min (Figures 1C and S2A). This change in maximal bead displacement is associated with a concurrent change in the spatial profile and range of the deformation and velocity fields (Figures 1B and S1E; Video S2). Our data show that the same localized force can lead to a significantly different deformation pattern when applied at developmental time points that differ by only a few minutes
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