Getting in shape: physical principles underlying order generation and shape change in the morphogenesis of thin tissues
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Getting in shape: physical principles underlying order generation and shape change in the morphogenesis of thin tissues


In plants and animals, developmental programs transform single-celled zygotes intofully formed and functional organisms. Understanding morphogenesis, the collective set of mechanisms that transduce discrete genetic information into the 3D form of tissues, organs, and appendages, is a foundational problem at the interface of biology and physics. While great progress has been made characterizing the molecular components that deter- mine the initial body plan, the subsequent dynamics of cellular rearrangements and tissue deformations that ultimately shape the organism are far less understood. A thorough de- scription of morphogenesis necessitates an understanding of the intricate interplay among genetics, mechanics, and geometry.

This dissertation presents a body of work aimed at understanding how mechanics andgeometry sculpt thin tissues into complex shapes during development. We apply a com- bination of theoretical, computational, and experimental methods to build quantitative descriptions of a variety of morphogenetic processes, including germband organization, organogenesis, and limb growth. In each setting, careful analysis reveals how physical mechanisms dynamically coordinate the self-organization of shape and form across mul- tiple scales, from the cellular to the organismal. The synthesis of these various results contributes towards building a quantitative and predictive understanding of morphogen- esis.

In Chapter 2, we present set of computational methods for the characterization andanalysis of tissue deformation in tubelike surfaces. These methods, contained within our open-source TubULAR package, enable users to extract dynamic surfaces, construct 2D parameterizations optimized for tracking tissue parcels, measure whole-organ tissue deformation, and compute signatures of 3D motion. We showcase the power of these methods by quantifying tissue flow during the development of the Drosophila midgut and the zebrafish heart. Decomposition of complicated flow fields in to simple components with straightforward physical interpretations enable novel insights that would be difficult or impossible to find with exisiting methodologies.

In Chapter 3, we demonstrate how actively oriented cell divisions organize the ecto-dermal germband in Parhyale hawaiensis. Live imaging and computer vision reveal that waves of cell proliferation sweep across the embryo in such a way that the initially fluid germband flows towards a fourfold orientationally ordered state. We develop a hydrody- namic model that can predict coarse-grained flow fields from division events, bridging the gap between cell-scale and tissue-scale dynamics. Vertex model simulations demonstrate that oriented cell divisions constitute a robust mechanism for generating orientational order in living tissues far from thermal equilibrium.

In Chapter 4, we study the transformation of the Drosophila midgut from a simpletube into a complex, coiling configuration of folds and compartments. We demonstrate that tissue shape is controlled by gene expression via mechanical interactions between heterologous tissue layers. Hox genes mediate calcium signaling that regulates muscle contractions at precise locations along the length of the gut. These muscle contractions induce sharp folds and convergent extenstion in the gut endoderm, which is strongly con- strained by tissue incompressibility. We show that the tissue scale flow is mediated by anisotropic cell shape change resulting from the mechanical coupling to muscle contractil- ity. Taken together, these results form a concrete link from genes to cell-scale mechanics to tissue morphodynamics via active forces.

In Chapter 5, we present a theoretical and computational framework for tacklingthe problem of growth pattern selection in epithelial morphogenesis. We show that de- velopmental programs can be quantified in terms of anistropy and areal growth rates. Arbitrarily complicated growth patterns can be built up by composing simple infinites- imal updates to the system’s intrinsic geometry. We proposed an action principle that selects for simple growth patterns that minimize spatiotemporal variation in these quan- tities. We then applied this formalism to seveal synthetic and experimental systems, including limb morphogenesis in Parhyale.

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