Tissue tension and not interphase cell shape determines cell division orientation in the Drosophila follicular epithelium

Abstract

We investigated the cell behaviors that drive morphogenesis of the Drosophila follicular epithelium during expansion and elongation of early‐stage egg chambers. We found that cell division is not required for elongation of the early follicular epithelium, but drives the tissue toward optimal geometric packing. We examined the orientation of cell divisions with respect to the planar tissue axis and found a bias toward the primary direction of tissue expansion. However, interphase cell shapes demonstrate the opposite bias. Hertwig's rule, which holds that cell elongation determines division orientation, is therefore broken in this tissue. This observation cannot be explained by the anisotropic activity of the conserved Pins/Mud spindle‐orienting machinery, which controls division orientation in the apical–basal axis and planar division orientation in other epithelial tissues. Rather, cortical tension at the apical surface translates into planar division orientation in a manner dependent on Canoe/Afadin, which links actomyosin to adherens junctions. These findings demonstrate that division orientation in different axes—apical–basal and planar—is controlled by distinct, independent mechanisms in a proliferating epithelium.

Getting into shape: tissue tension drives oriented cell divisions during organogenesis

“…In egg chambers, Finegan et al (2019) found that during the phase of biased division orientation, apical myosin coalesces in multicellular nodes, consistent with the idea that tissuelevel force is generated by myosin contractility. They first asked whether known differences in follicle cell shape and behavior at the poles versus at the equator (Alegot et al, 2018) reflect differences in tissue tension across these two areas.…”

“…In other tissues, tissue-level apical cortical tension is mediated by the actomyosin cytoskeletonanchored cell-cell by cell junctions; e.g., in germband-extending Drosophila embryos, planar-polarized multicellular myosin cables and oppositely planar-polarized junctional proteins drive cell rearrangements. In egg chambers, Finegan et al (2019) found that during the phase of biased division orientation, apical myosin coalesces in multicellular nodes, consistent with the idea that tissuelevel force is generated by myosin contractility. However, adherens junction proteins and the junction-cytoskeleton linker Canoe did not exhibit obvious planar polarity.…”

“…In other epithelial tissues, Canoe and its mammalian homolog Afadin aid in linking the actomyosin cytoskeleton to adherens junctions, mediating cellular responses to tension (Sawyer et al, 2011;Choi et al, 2016). Finegan et al (2019) found that after Canoe knockdown, myosin detached from cell-cell contacts, as was seen in other tissues, supporting a role in tension transmission across epithelia. Canoe knockdown also disrupted planar cell division bias.…”

“…Finegan et al (2019) use the simple model of the Drosophila ovary and elongation of each egg chamber to explore this process. Finegan et al (2019) use the simple model of the Drosophila ovary and elongation of each egg chamber to explore this process.…”

“…The shapes and architecture of the organs in the animal body develop through complex coordination of cell shape change, cell migration, and cell proliferation. Finegan et al (2019) use the simple model of the Drosophila ovary and elongation of each egg chamber to explore this process. They find that a gradient of myosin-driven tension exists along the axis of organ elongation and that this orients the division of the constituent cells.…”