Tissue folding promotes three-dimensional (3D) form during development. In many cases, folding is associated with myosin accumulation at the apical surface of epithelial cells, as seen in the vertebrate neural tube and the Drosophila ventral furrow. This type of folding is characterized by constriction of apical cell surfaces, and the resulting cell shape change is thought to cause tissue folding. Here, we use quantitative microscopy to measure the pattern of transcription, signaling, myosin activation and cell shape in the Drosophila mesoderm. We found that cells within the ventral domain accumulate different amounts of active apical non-muscle myosin 2 depending on the distance from the ventral midline. This gradient in active myosin depends on a newly quantified gradient in upstream signaling proteins. A 3D continuum model of the embryo with induced contractility demonstrates that contractility gradients, but not contractility per se, promote changes to surface curvature and folding. As predicted by the model, experimental broadening of the myosin domain in vivo disrupts tissue curvature where myosin is uniform. Our data argue that apical contractility gradients are important for tissue folding.
The authors declare no competing or financial interests.
Conceptualization: N.C.H., P.W.M., N.S., J.D., A.C.M.; Methodology: N.C.H., P.W.M., S.C., N.S., J.D., A.C.M.; Software: N.C.H., P.W.M.; Investigation: N.C.H., S.C.; Resources: N.C.H., S.C.; Writing - original draft: N.C.H., A.C.M.; Writing - review & editing: N.C.H., P.W.M., S.C., N.S., A.C.M.; Visualization: N.C.H., P.W.M., N.S.; Supervision: N.S., J.D., A.C.M.; Project administration: J.D., A.C.M.; Funding acquisition: J.D., A.C.M.
This work was funded by the National Institutes of Health (R01GM105984 to A.C.M.) and the American Cancer Society (125792-RSG-14-039-01-CSM to A.C.M.). This work was supported in part by the NIH Pre-Doctoral Training Grant T32GM007287. P.W.M. acknowledges financial support from Department of Defense (DoD) through the National Defense Science and Engineering Graduate Fellowship (NDSEG) Program. This work was supported by an Alfred P. Sloan Research Fellowship (to J.D.) and by a James S. McDonnell Foundation Complex Systems Scholar Award (to J.D.). Deposited in PMC for release after 12 months.
Supplementary information available online at http://dev.biologists.org/lookup/doi/10.1242/dev.146761.supplemental
- Received November 7, 2016.
- Accepted April 10, 2017.