Condensation of theDrosophilaNerve Cord is Oscillatory and depends on Coordinated Mechanical Interactions

Abstract

During development, organs must form with precise shapes and sizes. Organ morphology is not always obtained through growth; a classic counterexample is condensation of the nervous system during Drosophila embryogenesis. The mechanics underlying such condensation remain poorly understood. Here, we combine in toto live-imaging, biophysical and genetic perturbations, and atomic force microscopy to characterize the condensation of the Drosophila ventral nerve cord (VNC) during embryonic development at both subcellular and tissue scales. This analysis reveals that condensation is not a unidirectional continuous process, but instead occurs through oscillatory contractions alternating from anterior and posterior ends. The VNC mechanical properties spatially and temporally vary during its condensation, and forces along its longitudinal axis are spatially heterogeneous, with larger ones exerted between neuromeres. We demonstrate that the process of VNC condensation is dependent on the coordinated mechanical activities of neurons and glia. Finally, we show that these outcomes are consistent with a viscoelastic model of condensation, which incorporates time delays due to the different time scales on which the mechanical processes act, and effective frictional interactions. In summary, we have defined the complex and progressive mechanics driving VNC condensation, providing insights into how a highly viscous tissue can autonomously change shape and size.

Stability bounds of a delay visco-elastic rheological model with substrate friction

“…Although we are not aware of a experimental setup that may directly verify the bounds encountered, recent measurements of Drosophila condensation have correlated decaying deformation oscillations with a reduction in tissue viscosity (Karkali et al 2021), confirming the relation between oscillatory regime and visco-elastic material properties.…”

Scaling of internal organs during Drosophila embryonic development

“…Recent work has demonstrated that VNC condensation can be well described as a viscoelastic process, which generates oscillations in tissue length during condensation because of differences in the timescales over which the different mechanical interactions occur ( 41 ). Our work here shows that the VNC appears to only weakly scale with embryo length but does display evidence of a minimal viable size.…”

“…The hindgut offers an opportunity to test whether chiral tissues scale and, if so, whether they scale equally along different axes. The VNC is a unique organ that spans across the entire embryo length before condensing by means of apoptosis and long-range coordinated mechanical interactions ( 40 , 41 ). As the VNC shrinks, rather than grows, to its final size within the embryo, its mechanisms of size control are likely distinct from well-studied systems such as the Drosophila wing disk ( 12 ).…”