Maintenance of Organ Morphology via Regulation of Tissue Material Properties in the Drosophila Retina

Tissue morphologies generated in development must be structurally suited to their physiological function. Towards this end, developing organs enact both tissue-scale deformation programs that produce complex 3-dimensional shapes and cellular morphogenesis processes that spatially pattern assemblies of specialized cell and generate fate specific cellular structures. Whether these structural changes, happening at both the tissue and cellular scale, are synergistically coordinated or happen largely independent of each other in specific biological contexts remains an important unanswered question. During the development of the Drosophila retina, which is generated from an originally simple epithelial sheet, a tissue-scale curvature is acquired that is required for resolution of the visual system. Additionally, cell-type specific optical structures are generated that require extensive cellular remodeling. How these two processes influence each other in development to produce the final retina structure is an open question. The Drosophila retina is a compound eye composed of discrete, multicellular optical units, called ommatidia, that tile across the curved surface of the retina. Ommatidia undergo a dramatic elongation process that increases the apical-basal depth of the tissue ~5-fold. This elongation process coincides with an enrichment of actomyosin stress fibers at the basal surface of the retinal epithelium that have long been hypothesized to also generate retinal curvature. In this dissertation, I investigate the origins of retinal curvature, to temporally place this tissue morphogenesis process in the context of other cellular morphogenesis programs in the retina. I will first demonstrate that tissue-scale curvature is acquired long before ommatidial elongation, challenging current views of retinal morphogenesis. Retinal curvature is acquired earlier in development and temporally overlaps with an increase in the material rigidity of the tissue. I will demonstrate that increased tissue rigidity is required to maintain retinal curvature and discuss how this finding raises the possibility that curvature is induced via tissue extrinsic forces. Next, I will show that this increase in tissue rigidity is driven specifically by interommatidial pigment cells (IOPCs). Tissue rigidity is generated via increased IOPC junctional tension downstream of Rok-mediated actomyosin contractility, and tension is transmitted throughout a supracellular network comprised of apical actomyosin networks and mechanically coupled adherens junction complexes. Tension transmission is critical to bridge the cell and tissue scales, allowing uniform modulation of material rigidity across the expanse of the retinal epithelium. With the discovery that retinal curvature is acquired independent of tissue elongation, I then investigated how individual cellular morphogenesis events are controlled, such that larger tissue structure is maintained. In this work, it was found that mechanical interactions between discrete subpopulations of retinal cells helped maintain tissue integrity during the later cellular morphogenesis programs that elaborate specialized optical structures subsequent to curvature establishment. Taken together, these two studies highlight that the physical state of a given tissue may be employed both to leverage active forces towards generating functional morphologies and buffer forces resulting from distinct cellular morphogenesis programs to preserve overall tissue form.