Bulletin of the American Physical Society
APS March Meeting 2023
Volume 68, Number 3
Las Vegas, Nevada (March 5-10)
Virtual (March 20-22); Time Zone: Pacific Time
Session Y11: Morphogenesis IIFocus
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Sponsoring Units: DBIO Chair: Maryam Kohram, Princeton University Room: Room 203 |
Friday, March 10, 2023 8:00AM - 8:12AM |
Y11.00001: Modeling and Analysis of Mesophyll Tissue Development in Leaves and Flowers Across Species Arthur K MacKeith, Allison E Culbert, John D Treado, Adam B Roddy, Craig Brodersen, Mark D Shattuck, Corey S O'Hern Mesophyll tissue in plant leaves plays a critical role in providing mechanical stability and facilitating photosynthesis and displays a wide range of structural variation across species. However, little is known about the development of this tissue in three dimensions (3D). Early in development, the cells in mesophyll tissue are confluent. However, in mature leaves, the mesophyll tissue can either remain extremely dense or possess very dilute packing fractions comparable to highly porous gels. We hypothesize that the differences in the structural properties of mesophyll tissue are primarily driven by differences in cell stiffness, growth rate, and adhesion. We analyze 3D x-ray micro-computed tomography (microCT) scans of several species and quantify the variations in structure of the mesophyll during development and across species. We have also developed 3D deformable particle simulations to model mesophyll tissue development. We compare the results for the average shape parameter of the cells versus the porosity of mesophyll tissue in simulations and those observed in the microCT scans. Finally, we illustrate the variation in the physical properties of the cells that are required to recover the wide variation in mesophyll structural properties. |
Friday, March 10, 2023 8:12AM - 8:24AM |
Y11.00002: A hybrid model framework for studying mechanics of epithelial morphogenesis Joseph Sutlive, Tony Zhang, Bing He, Zi Chen Embryonic morphogenesis requires many stages of complex bending, twisting, and positioning of tissues as the organism develops. These coordinated movements often require complex coordination and regulation of biomechanical forces, the nature of which is often not well understood. Here we present a simulation framework for modeling morphogenetic events in early embryogenesis from a mechanics perspective. To accomplish this, we have implemented a hybrid model, which takes advantage of the benefits of vertex models and particle models while avoiding their respective drawbacks. We represent each cell membrane as a polygon consisting of a given number of nodes with elastic springs forming the polygon’s edges. Cells can then be assigned additional force components which act on the cell’s nodes such as forces originating from apical constriction. Additionally, we use a simple collision method implementing a ray casting algorithm to handle cell-cell collisions. The model has been used to successfully model the folding of mesoderm epithelium during Drosophila gastrulation and has illustrated how changing mechanical properties of cells can lead to “mutant” varieties. We further anticipate that the simplicity in development of new physics components and models using this framework will lead to its application to model several different morphogenetic events as well as allowing for identification of the regulatory role of mechanical forces in development. |
Friday, March 10, 2023 8:24AM - 8:36AM |
Y11.00003: Epithelial geometry reveals how positive tension feedback drives active cell intercalations during tissue convergence extension: Theory Nikolas H Claussen, Fridtjof Brauns, Matthew F Lefebvre, Sebastian J Streichan, Boris I Shraiman
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Friday, March 10, 2023 8:36AM - 8:48AM |
Y11.00004: Epithelial geometry reveals how positive tension feedback drives active cell intercalations during tissue convergence extension: Experiment Fridtjof Brauns, Nikolas H Claussen, Matthew F Lefebvre, Sebastian J Streichan, Boris I Shraiman Morphogenesis often involves tissue-scale flows (plastic deformations) which require cell rearrangements (cell neighbor exchanges/intercalations). In a passive fluid, these rearrangements are driven by external forces. In contrast, in a living tissue, internally stresses generated by molecular motors can drive active intercalations. Using gastrulation of drosophila embryos as a model system, imaged, segmented, and tracked in toto, we show how tension inference can be used to distinguish between these two processes purely based on the local geometry of the cell array. Active intercalations are characterized by an increasing (relative) tension on the collapsing cell junction, while junction collapse in passive intercalations takes place under constant tension. Geometrically, junctional tensions are reflected in the angles between junctions at each vertex. This suggests a novel decomposition of tissue strain rate into a contribution reflecting changes in the junction angles reflecting changing tensions and an isogonal (angle preserving) contribution. This decomposition systematically links the tissue level dynamics to the cell/junction level dynamics. Moreover, the ensemble statistics of the tensions (i.e. angles) at each vertex allows us to robustly characterize the cell-scale mechanical state of the tissue. Our findings inform a minimal model based on positive tension feedback which reproduces the experimental observations and explains the coordination of subcellular stress generation underlying coherent tissue level flows. |
Friday, March 10, 2023 8:48AM - 9:24AM |
Y11.00005: From genes to geometry: how a visceral organ takes form Invited Speaker: Noah P Mitchell During morphogenesis, tissues fold into complex shapes to form visceral organs. Genetic signals are known to govern form, but the mechanical processes by which interacting tissue layers generate vital organ shapes remain elusive. Here, we trace an organ's in toto dynamics and uncover the mechanical interactions across tissue layers, from sub-cellular to organ scale. Using deep tissue light-sheet microscopy for whole-organ live imaging, we find a mechanical program folding the embryonic midgut of Drosophila: hox genes control the emergence of high-frequency calcium pulses, which trigger muscle contractions. These contractions, in turn, induce cell shape change in the adjacent tissue layer, collectively driving a pattern of convergent extension. Analysis of the kinematics shows that patterned convergent extension (ie, in-plane shear) is linked to out-of-plane organ folding. These findings offer a mechanical route for gene expression to induce organ shape change: genetic patterning in one layer triggers a physical process in the adjacent layer to drive organ shape change. |
Friday, March 10, 2023 9:24AM - 9:36AM |
Y11.00006: Modeling cell shape changes in the zebrafish embryo using a 3D vertex model Raj Kumar Manna, Emma M Retzlaff, Elizabeth Lawson-Keister, Michael Bates, Yiling Lan, Heidi Hehnly, Jeffrey D Amack, M Lisa L Manning Programmed cell shape changes in a developing embryo are essential for building many functional organs such as the neural tube, gut, and heart. Here we focus on Kupffer’s vesicle (KV) in the zebrafish embryo as a model organ, as it undergoes programmed asymmetric cell shape changes to establish the left-right axis of the embryo. A 3D Voronoi model, where the degrees of freedom are the cell centers, has previously demonstrated that the tailbud tissue surrounding the KV can generate drag forces and drive cell shape changes in KV. However, recent work has suggested that a 3D Vertex model, where the degrees of freedom are the vertices between cells, better captures realistic shape changes in systems with heterogenous architectures like the KV. Here we employ the 3D Vertex model to capture the propulsion of KV through tailbud tissue and study cell shape changes. We investigate KV cell shapes and cell distribution for a range of values of tailbud tissue fluidity and KV propulsion velocity, and compare to experiments. We further examine how the left-right asymmetric tailbud tissue mechanics, notochord-KV interaction, and differential propulsion of cells in KV influence the cell shape changes in KV. Our findings provide insight into the physical mechanisms that regulate organogenesis, and may help identify new targets for therapeutics. |
Friday, March 10, 2023 9:36AM - 9:48AM |
Y11.00007: 3D cell packing dynamics in converging and extending epithelial sheets Sassan Ostvar, Erika Kusaka, Xun Wang, Alyssa Lesko, Ann Sutherland, Karen E Kasza Epithelial sheets can realize diverse shapes by deforming and rearranging their constituent cells along specific motifs in space and time. During early embryonic development, major tissue shape changes often occur in bursts of activity, when endogenous and/or exogenous forces induce transient states of rapid internal reorganization, or fluidity. The “self-sculpting” motion of fluidizing tissues is facilitated by changes in tissue rheology that are linked to the transient local structure of cell packings. The 3D dynamics of cell packings in epithelial sheets and their contribution to global deformations remain to be fully understood. Here we study cell shape changes and rearrangements in two model tissues undergoing convergent extension flows: the mouse neural plate, a proliferating pseudostratified epithelium, and the fruit fly germband, a non-proliferating columnar epithelium. In both systems, we observe gradients in cell shapes and alignment along the apical-to-basal axis, indicative of distinct basal and apical tissue flows. Mutations that disrupt cytoskeletal machineries have distinct effects along the apical-basal axis and lead to measurable changes in global tissue flow and curvature. Coordination of apical and basal tissue flows via 3D cell shape changes and rearrangements appears to be critical for epithelial sheets to properly achieve their morphogenetic targets with implications for understanding developmental defects rooted in aberrant tissue mechanics during morphogenesis. |
Friday, March 10, 2023 9:48AM - 10:00AM |
Y11.00008: Activity and topological defects in 3D morphogenesis Richard D Ho, Luiza Angheluta-Bauer During morphogenesis, a group of cells can change shape and orientation, including breaking previous global symmetry. Simulations of this process often impose this symmetry breaking on the system, whereas we would like to make these changes emergent from the evolution of the individual cells. We extend a previously developed discrete 3D cell model, which can capture cell morphological effects such as budding, gastrulation, and neurulation. This model couples the evolution equations of two polarities and position and its simplicity allows the simulation of thousands of interacting cells at reasonable computational cost. We now extend it to include the presence of a diffusive chemical agent, activity, and parameter dependence on topological defects in polarity. With a particular interest on how these results relate to organoids, we examine the presence of these effects on the morphological changes. |
Friday, March 10, 2023 10:00AM - 10:12AM |
Y11.00009: A mechanochemical model recapitulates distinct vertebrate gastrulation modes Mattia Serra During vertebrate gastrulation, an embryo transforms from a layer of epithelial cells into a multilayered gastrula. This process requires the coordinated movements of hundreds to tens of thousands of cells, depending on the organism. In the chick, patterns of myosin cables spanning several cells drive coordinated tissue flows. How this coordinated activity emerges and spatially evolves into large-scale patterns in a developing organism remains unresolved. We derive a minimal theoretical framework that couples actomyosin activity to tissue flows, thus providing the basis for gastrulation dynamics. Our model predicts the onset and development of gastrulation flows in normal and experimentally perturbed chick embryos as a spontaneous instability. Varying the initial conditions and a critical parameter associated with active cell ingression, our model recapitulates the phase space of gastrulation morphologies seen across vertebrates, consistent with experiments. Altogether, our results suggest that relatively small changes in the organization of critical cell behaviors associated with different force-generating mechanisms contribute to distinct vertebrate gastrulation modes via an evolvable self-organizing mechanochemical process. |
Friday, March 10, 2023 10:12AM - 10:24AM |
Y11.00010: Branching morphogenesis of sea cucumber ossicles in multi-cellular syncytial confinement Pranav Vyas, Charlotte Brannon, Laurent Formery, Christopher Lowe, Manu Prakash Biomineralization is in living systems and has remained elusive due to limitations in the simultaneous understanding of both physical and biomolecular processes. In holothurians, biomineralization occurs in the form of discrete ~100 um length scale structures called ossicles that diversify in shapes not only across species but even within an individual animal. Through live and fixed microscopy techniques, we establish that these structures grow from individual crystalline seeds inside a multi-cell syncytial complex with the biomineralized phase completely covered with a membrane-coated cytoplasmic sheath. We demonstrate that the initial seed transforms into a multi-holed structure through 4 key steps - instability in the seed, tip extension, tip splitting, and merging of two tips. Through large-scale statistics on microCT data, we probe the robustness of the processes described. Throughout the growth, we demonstrate that cytoplasmic and membranous activity restricted to the surface of the biomineralized phase rather than motility of participating cell bodies regulate the material transport and directional growth of the structure. By observing distinct developmental niches, we demonstrate differential symmetry breaking and seed cell-cluster dispersion as the structure grows, which acts as an additional layer of control. The system thus serves as a unique playground merging non-equilibrium solidification growth in melts/solutions and classical branching morphogenesis in living systems. |
Friday, March 10, 2023 10:24AM - 10:36AM |
Y11.00011: Recording symmetry breaking during gastruloid morphogenesis with recombinase circuits Harold M McNamara, Jared Toettcher In vitro models of embryonic development and organogenesis have revealed the remarkable potential of stem cells to self-organize morphogenesis. While great progress has been made towards measuring the complexity of organoid morphologies and cell types, we have a less complete understanding of how signaling dynamics orchestrate this emergent biological complexity. |
Friday, March 10, 2023 10:36AM - 10:48AM |
Y11.00012: Pushing the envelope: force balance between the spindle and nuclear envelope during fission yeast closed mitosis Marcus A Begley, Christian Pagán Medina, Parsa Zareiesfandabadi, Matthew Rapp, Abhimanyu Sharma, Mary W Elting When eukaryotic cells divide, the chromosomes must be duplicated and segregated into two new daughter nuclei, each of which are isolated from the cytoplasm by the nuclear envelope. The mitotic spindle has the critical task of segregating chromosomes. To do so, it must self-assemble and then generate force to pull chromosomes to the right place at the right time. In many eukaryotes, the nuclear envelope breaks down during this process, while in others, chromosome segregation happens inside an intact nuclear envelope. In the fission yeast S. pombe, which has closed mitosis, changes to nuclear envelope shape and topology accompany spindle elongation. While it is assumed that this elongation drives nuclear shape changes, the mechanics underlying these transitions are very poorly understood. To probe this question, we molecularly and mechanically perturb mitotic S. pombe cells. We sever specific mitotic structures, including the spindle and the nuclear envelope, by laser ablation, and we quantify the subsequent response to these acute perturbations using live cell confocal microscopy. The dynamics of these responses report on the material properties of the spindle, nuclear envelope, and the nucleoplasm. We perform a similar set of experiments in S. japonicus, the phylogenetic cousin of S. pombe, which goes through semi-open mitosis, in which nuclear envelope closure is not required. We find differences in spindle mechanics between the two species, suggesting how features of spindle organization may evolve to match their mechanical constraints. |
Friday, March 10, 2023 10:48AM - 11:00AM |
Y11.00013: Modeling the spongy mesophyll in plant leaves in three dimensions Allison E Culbert, Arthur K MacKeith, Adam B Roddy, Corey S O'Hern, Mark D Shattuck Mature spongy mesophyll tissue in plant leaves is a complex porous network of highly non-spherical cells. The mesophyll tissue provides mechanical stability for the leaf, as well as allowing CO2 to reach the chloroplasts for photosynthesis. Recent numerical simulations in two dimensions have shown that mesophyll tissue development in Arabidopsis thaliana can be modeled as a self-assembly process, where originally dense collections of cells grow into void space giving rise to non-spherical cells in porous networks that can maintain fixed positive external pressure. In this work, we perform structural characterizations of mature mesophyll tissues using micro-CT scans from multiple species. We focus on quantifying the porosity, cell shape, and density correlations in these tissue scans. In addition, we have developed a three-dimensional discrete element method simulation of mesophyll tissue and will compare the structural properties obtained from the simulations to those found in the micro-CT scans. |
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