Bulletin of the American Physical Society
APS March Meeting 2021
Volume 66, Number 1
Monday–Friday, March 15–19, 2021; Virtual; Time Zone: Central Daylight Time, USA
Session R11: Morphogenesis IIFocus Live
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Sponsoring Units: DBIO Chair: Zi Chen, Dartmouth College; Smitha Vishveshwara, University of Illinois Urbana-Champaign |
Thursday, March 18, 2021 8:00AM - 8:36AM Live |
R11.00001: Patterned morphogenesis of epithelial wound detection and healing Invited Speaker: Shane Hutson When a sheet of epithelial cells is wounded, cells around the wound are recruited from a near quiescent state to reactivate motility and proliferation behaviors similar to early development. Importantly, the epithelium around the wound must be appropriately patterned to drive different cell behaviors in proximal and distal regions. As the first stage of this patterning, surrounding epithelial cells undergo a dramatic increase in cytosolic calcium. This increase occurs quickly: calcium floods into damaged cells within 0.1 s, moves into adjacent cells over ~20 s, and appears in a much larger set of surrounding cells via a delayed second expansion over 40-300 s. Nonetheless, increased calcium is a reporter; cells must detect wounds even earlier. Using the calcium response as a proxy for wound detection, we identify an upstream G-protein-coupled-receptor (GPCR) signaling pathway, including the receptor and its protease-activated chemokine ligand. We present experimental and computational evidence delineating the mechanisms by which the calcium signaling patterns are established and through which cells interpret the calcium signals to drive wound repair behaviors. |
Thursday, March 18, 2021 8:36AM - 8:48AM Live |
R11.00002: Precision in a rush: decision making in early fly development Jonathan J Desponds, Massimo Vergassola, Aleksandra Walczak Despite very limited time, organisms develop in reproducible ways. In the early stages of fly development positional information is read out in a few minutes to produce steep and precise gene expression patterns — the rough blueprint for future body parts. Motivated by recent live imaging experiments in fly embryos, I will discuss the speed-accuracy trade-offs. Traditional arguments based on fixed-time sampling of Bicoid concentration indicate that an accurate readout is not possible within the short times observed experimentally. I will compare fixed-time sampling strategies to decisions made on-the-fly, which are based on updating and comparing the likelihoods of being at an anterior or a posterior location. I will show that these more efficient schemes can complete reliable cell fate decisions even within the very short embryological timescales and discuss the the role of promoter architectures on the mean decision time. |
Thursday, March 18, 2021 8:48AM - 9:00AM Live |
R11.00003: The Role of Environment, Material, and Regulatory Function in the Morphological Diversity of Termite Mounds Tadeu Fagundes, Juan Ordonez, Neda Yaghoobian Most termites around the globe build massive structures that are of several orders of magnitudes larger than themselves. These superstructures, called termite mounds, passively regulate their internal environments and provide ideal living conditions for their residing termites. Termite mounds exhibit systematic structural designs that vary in size and shape among species and locations. While most previous efforts explored the regulatory functions of termite mounds, only a few studies investigated the physics behind their morphological diversity. To explain the different but systematic shapes of termite mounds, this work develops a computational model to investigate the connection between the mound’s structural form and the mounds’ local environment, material, and regulatory functions. Using the fundamentals of heat transfer, the model captures the main structural features observed in natural termite mounds. The influence of the environmental factors and mound function over the structural form is analyzed thoroughly. The proposed methodology can be extended to the prediction of the architecture of natural systems for which the structural and environmental information can be attained. |
Thursday, March 18, 2021 9:00AM - 9:12AM Live |
R11.00004: Collective cell mechanics of epithelial shells with organoid-like morphologies Jan Rozman, Matej Krajnc, Primoz Ziherl The study of organoids, artificially grown cell aggregates with the functionality and small-scale anatomy of real organs, is one of the most active areas of research in biology and biophysics, yet the basic physical origins of their different morphologies remain poorly understood. Here, we propose a mechanistic theory of epithelial shells which resemble small-organoid morphologies. Using a 3D surface tension-based vertex model, we reproduce the characteristic shapes from branched and budded to invaginated structures. We find that the formation of branched morphologies relies strongly on junctional activity, enabling temporary aggregations of topological defects in cell packing. To elucidate our numerical results, we develop an effective elasticity theory, which allows one to estimate the apico-basal polarity from the tissue-scale modulation of cell height. Our work provides a generic interpretation of the observed epithelial shell morphologies, highlighting the role of physical factors such as differential surface tension, cell rearrangements, and tissue growth. |
Thursday, March 18, 2021 9:12AM - 9:24AM Live |
R11.00005: Cellular Fourier Transform: a new approach to analyse living tissues at multiple scales Antoine Fruleux, Arezki Boudaoud Many questions in Biology concern the relation between different scales (i.e. sub-cellular, cellular or supra-cellular). For example, organ development often gives rise to robust sizes and shapes, in striking contrast with the variability observed at a cellular scale. In a classical physical context, many tools exist to investigate the relation between scales such as Fourier Transforms or wavelet decomposition but they are not well suited to biological tissues. In biological tissues, cells set a reference scale at which parameters and fields reflecting material properties and state are often assessed and space discretization based on standard coordinate systems is not commensurate with the natural discretization into geometrically disordered cells. We built a method, which we call Cellular Fourier Transform (CFT), to analyze cellular fields, which includes both discrete fields defined only at cell level and continuous fields smoothed out from their sub-cell variations. During my presentation, I will introduce the method and discuss its application to the growth of floral organs. |
Thursday, March 18, 2021 9:24AM - 9:36AM Live |
R11.00006: Theory of branching morphogenesis via local interactions and global cues Mehmet Can Ucar, Dimitrii Kamenev, Dominik Fachet, Saida Hadjab, Edouard Hannezo Branching morphogenesis governs the formation of many organs such as lung, kidney, and the neurovascular system. Many studies have recently explored system-specific molecular and cellular regulatory mechanisms underlying single branching events. However, how large-scale tree structure arises from local interactions remains unclear. In particular, the respective role of stochasticity, self-organizing rules, and global cues such as guidance or repulsion in allowing for robust tissue growth is often poorly defined. Here, we develop a theoretical framework to describe a stochastic and self-organized branching process in the presence of external guidance, based on branching and annihilating random walks in an external potential. Using a continuum model for the angular alignment of branch segments with an external field, we quantitatively predict signatures of external guidance vs. local rules, such as angle distributions and the area invaded by the branched networks. We compare our theoretical results with experimental data on innervation of the zebrafish caudal fin and find good quantitative agreement. Our model provides a generic framework to explore directed tissue growth at different scales ranging from neuronal branching to epithelial branching such as in sprouting angiogenesis. |
Thursday, March 18, 2021 9:36AM - 9:48AM Live |
R11.00007: Stability of oriented deformation in developing biological tissues Muhamet Ibrahimi, Matthias Merkel In polar and nematic active materials, the homogeneously deforming state exhibits a well-known instability. Meanwhile, during development of multicellular animals, tissues often undergo oriented deformation processes that are robust. How can such deformation be stable despite the known active matter instability? Here, we explore a scenario where the gradient of a scalar field defines active anisotropic stresses in the system. This is motivated by the existence of molecular concentration fields that can control biological tissue deformation during development (e.g. “morphogen gradients”). We find that the homogeneously deforming state is stable in the extensile case, but unstable in the contractile case. Intriguingly, while there are several examples for extensile tissues in nature, we could so far not identify any example for the contractile case. Hence, our results point to a potential new developmental principle in biology that is directly rooted in active matter physics. |
Thursday, March 18, 2021 9:48AM - 10:00AM Live |
R11.00008: Detecting bifurcations in tissue development Simon Freedman, Bingxian Xu, Sidhartha Goyal, Madhav Mani During embryonic development, pluripotent cells undergo fate transitions, yielding functionally specialized cells. These transitions are often visualized as bifurcations, points in time when the landscape of cell fates changes from having one steady state to multiple, or different steady states. Experimental tools such as single-cell RNA sequencing, which measures the full distribution of a cell’s possible genetic compositions, can be used to obtain trajectories of gene expression during a developmental transition, but it remains unclear how RNA dynamics relate to changes in cellular state space. We show that bifurcations in cellular state space can be analytically pinpointed and qualitatively assessed directly from the temporal covariance of gene expression. We apply our bifurcation time measurement to a well characterized sequence of cell fate decisions, the transition of hematopoietic stem cells to neutrophils, to identify genes that drive fate decisions. Our work provides a robust mathematical framework for categorizing developmental transitions that can aid in gene network inference and help determine features of cell differentiation, such as when and why cell fate transitions are reversible or generate multiple cell types. |
Thursday, March 18, 2021 10:00AM - 10:12AM Live |
R11.00009: Spontaneous strains in tissue mechanics: topologically driven morphogenesis Carlos Duque, Carl D Modes, Frank Jülicher Growth processes are widely used by biological tissue in order to undergo shape changes. It has been determined that one of the reshaping mechanisms relies on the spontaneous strains that arise within the tissue as a result of gradients of growth. In some cases, the tissue can alleviate the induced internal stresses by adopting intricate 3D configurations as has been extensively reported, for example, in various plant tissue. However, less is understood about the formation of spontaneous strains in the much more dynamic animal tissue. Recent observations of morphogenic events together with single-cell resolution imaging have revealed that a variety of tissue such as the Drosophila melanogaster wing and embryo form as a result of cell elongation, proliferation, and division. The coupling of these cellular events is translated into gradients of the stress-field of the tissue that promote shape changes. Here, we seek to make a connection between cellular events and the physics of shape-changing materials based on the elongation and contraction of nematic elastomers. Furthermore, we discuss a coarse-grained model for morphogenesis a la physics of nematic liquid crystals that builds on the proliferation and dynamics of topological defects. |
Thursday, March 18, 2021 10:12AM - 10:24AM Live |
R11.00010: Patterned shear flows drive folding during organogenesis Noah Mitchell, Dillon Cislo, Suraj Shankar, Zvonimir Dogic, Boris I Shraiman, Sebastian Streichan In morphogenesis, living matter translates information encoded at the cellular scale into complex shape transformations. How does in-plane tissue patterning generate out-of-plane deformation needed to sculpt complex forms? A dramatic example of this theme is the fruit fly midgut -- a tube that folds and coils into a helical configuration in only two hours. Here, using a combination of light-sheet microscopy, genetics, computer vision, and tissue cartography, we reconstruct the full 3D shape dynamics and identify the driving sources of the shape change by linking out-of-plane motion to the cellular flow and active contraction patterns. Optogenetic manipulation of contractility in the endoderm and muscle layers decouples the role of each in sculpting the bilayer organ, enabling a simple mechanical model for midgut morphogenesis. |
Thursday, March 18, 2021 10:24AM - 10:36AM Live |
R11.00011: The role of tissue mechanics in symmetry breaking during organogenesis in the zebrafish embryo Paula Sanematsu, Gonca Erdemci-Tandogan, Matthias Merkel, Himani Patel, Jeffrey Amack, M Lisa Manning The left-right (LR) patterning of internal organs in a vertebrate is vital to its function, and defects in patterning are associated with congenital disease. In the zebrafish embryo, Kupffer’s vesicle (KV) is a transient organ that acts as the LR organizer. As the KV moves through the tailbud, KV cells change shape differently on the anterior and posterior sides of the organ, resulting in an asymmetric distribution of cilia. While such distribution is necessary for establishing LR asymmetry, the upstream changes in cell shape remain poorly understood. Extensive searches for biochemical signaling that may regulate KV architecture have not been fruitful. Here, we take a different approach by analyzing how mechanical drag forces on the KV generated by surrounding tailbud tissue can contribute to asymmetry. We develop a full 3D vertex model of the tissue architecture, instead of the usual 2D models, to better quantify the 3D forces at play. Velocity gradients obtained by particle image velocimetry (PIV) analysis of zebrafish embryos, along with model-based calculations of shear stresses and pressure acting on KV, indicate that tissue-scale mechanical forces are exerted on the KV, and may help drive cell shape changes. |
Thursday, March 18, 2021 10:36AM - 10:48AM Live |
R11.00012: Origin of symmetry breaking underlying polarized flow during Drosophila endoderm morphogenesis Emily Gehrels, Bandan Chakrabortty, Matthias Merkel, Thomas Lecuit The invagination of the Drosophila endoderm is driven by a complex interplay between biological signaling and tissue mechanics. Using several live imaging techniques, we are able to observe how changes in myosin levels, tissue curvature, and adhesion between the epithelium and the vitelline membrane relate to tissue dynamics during the process of endoderm morphogenesis. We then challenge our initial hypotheses through the use of selected genetic perturbations of the embryos combined with theoretical/computational methods to model the behavior of the tissue. With this combination of experimental and modeling approaches, we aim to systematically unravel how organized multicellular dynamics emerge from genetic, mechanical, and geometric "information", and feedback during morphogenesis. This work will shed new light on a variety of morphogenetic processes occurring during development. |
Thursday, March 18, 2021 10:48AM - 11:00AM Live |
R11.00013: Morphogenesis of silica microstructures in diatoms Maria Feofilova, Eric R Dufresne Diatoms are single-cell organisms with a remarkable cell wall called the diatom frustule. The frustule is made of multi-scale micro- and nano-patterned silica. The cell wall's intricate structure has puzzled scientists for quite some time. While a lot has recently been learned about the synthetic pathways that produce silica, still little is known about how the distinct hierarchical structure of the frustule is formed. |
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