Cell and tissue mechanics in 3-D organ morphogenesis: Insights from Drosophila pupal retina development

Morphogenesis requires dynamic changes in cell and tissue mechanics. Because organs are complex multi-cellular structures that develop slowly, understanding how they acquire their unique 3-D forms requires in vivo experimental systems that can bridge the discrete processes that occur at different physical-scales, from cell, to tissue, to multi-organ, and at different time-scales, from minutes, to hours, to days. The challenge of establishing causal relationships across scales has limited exploration of the cell biological processes that collectively produce the changes in tissue material properties and mechanics required for developing epithelia to deform in stereotyped ways. In this review, we discuss recent work focused on the Drosophila pupal retina that has begun to fill this gap. The new findings collectively emphasize how supracellular networks can channel mechanical outputs generated from rapid, cytoskeletal/junctional dynamics into the organized changes in tissue-scale material properties and mechanics needed to produce functional 3-D organ morphologies. By linking cellular dynamics with tissue-scale mechanics, supracellular networks may also critically determine how tissue-extrinsic forces from the growth environment contribute to programmed shape deformations that occur during morphogenesis. The mechanisms that emerge from this collective body of work provide a valuable conceptual framework for considering how cell and tissue mechanics, working in combination with environmental forces and tissue-intrinsic force generation programs, may instruct and constrain 3-D morphologies across a broad range of biological contexts.