Dynamic interplay of protrusive microtubule and contractile actomyosin forces drives tissue extension

Abstract

In order to shape a tissue, cell-based mechanical forces have to be integrated into global force patterns. Over the last decades, the importance of actomyosin contractile arrays, which are the key constituents of various morphogenetic processes, has been established for many tissues. Intriguingly, recent studies demonstrate that the microtubule cytoskeleton mediates folding and elongation of the epithelial sheet during Drosophila morphogenesis, placing microtubule mechanics en par with actin-based processes. While these studies establish the importance of both cytoskeletal systems during cell and tissue rearrangements, a mechanistic explanation of their functional hierarchy is currently missing. Here, we dissect the individual roles of these two key generators of mechanical forces during epithelium elongation. We demonstrate that microtubules dictate cell shape changes and actomyosin refines them. Combining experimental and numerical approaches, we find that altering the microtubule and actomyosin functions results in predictable changes in tissue shape. We further show that planar polarized microtubule patterning is independent of cell geometry and actomyosin-based mechanics. These results support a hierarchical mechanism, whereby microtubule-based forces in some epithelial systems prime actomyosin-generated forces.