Bulletin of the American Physical Society
APS March Meeting 2022
Volume 67, Number 3
Monday–Friday, March 14–18, 2022; Chicago
Session K05: Morphogenesis IIRecordings Available
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Sponsoring Units: DBIO Chair: Andrej Kosmrlj, Princeton Room: McCormick Place W-178A |
Tuesday, March 15, 2022 3:00PM - 3:12PM |
K05.00001: Global Constraints within the Developmental Program of the Drosophila Wing Vasyl Alba, James E Carthew, Richard Carthew, Madhav Mani Organismal phenotypes emerge from a complex set of genotypic interactions. While technological advances in sequencing provide a quantitative description of an organism’s genotype, characterization of an organism’s physical phenotype lags far behind. Here, we relate genotype to the complex and multi-dimensional phenotype of an anatomical structure using the Drosophila wing as a model system. We develop a mathematical approach that enables a robust description of biologically salient phenotypic variation. Analysing natural phenotypic variation, and variation generated by weak perturbations in genetic and environmental conditions during development, we observe a highly constrained set of wing phenotypes. In a striking example of dimensionality reduction, the nature of varieties produced by the Drosophila developmental program is constrained to a single integrated mode of variation in the wing. Our strategy demonstrates the emergent simplicity manifest in the genotype-to-phenotype map in the Drosophila wing and may represent a general approach for interrogating a variety of genotype-phenotype relationships. |
Tuesday, March 15, 2022 3:12PM - 3:24PM |
K05.00002: Mechanical feedback in Drosophila embryonic development Nikolas H Claussen, Matthew F Lefebvre, Hannah J Gustavson, Noah P Mitchell, Stefano De Renzis, Boris I Shraiman, Sebastian J Streichan Morphogenesis, the forming organism shape, raises deep questions in biology and physics. Two principles coordinate morphogenetic force-generation: genetic programs and dynamic response to mechanical stimuli. Any understanding requires disentangling them, which is challenging. We address this in the D. melanogaster embryo, combining in-toto imaging, (opto-)genetic perturbations, and quantitative modeling. During convergent extension (CE), a fundamental developmental motive, non-muscle myosin II is recruited to cell-cell junctions to generate forces. Myosin gradients drive tissue flow. Previous work linked myosin to the pattern of the so-called pair-rule genes. We show that at the onset of CE, myosin is recruited by mechano-sensation in proportion to the strain rate, a long-range effect establishing the initial myosin gradient. The effect’s strength is spatially graded, possibly via genetics. Next, as tissue flows, gene patterns deform yet myosin anisotropy remains aligned to a static source, potentially tension. Factoring in the time myosin is bound to junctions, we can describe the dynamics of the anisotropy orientation. Our results indicate mechanical feedback regulates embryo-scale cytoskeletal organization and tissue flow, casting CE as an autonomous, self-organized process. |
Tuesday, March 15, 2022 3:24PM - 3:36PM |
K05.00003: Physical mechanisms of tissue compartmentalization andinternalizationin the Drosophila embryo Gonca Erdemci-Tandogan, Jessica C Yu, Negar Balaghi, Veronica Castle, Rodrigo Fernandez-Gonzalez Compartment boundaries prevent cell mixing during embryonic development. Cables formed by actin and the molecular motor myosin II are often found at compartment boundaries. How boundaries are established and maintained remains unclear. In the Drosophila embryo, the mesectoderm separates ectoderm and mesoderm, forming the ventral midline. Eventually, mesectoderm cells are internalized becoming part of the central nervous system. We found that ectoderm and mesectoderm remained separated as the mesectoderm was internalized, suggesting the presence of a boundary between the tissues. Using live microscopy, we found an enrichment of myosin at the mesectoderm-ectoderm boundary (MEB), forming a supracellular cable. Myosin levels at the MEB decreased as the mesectoderm was internalized. To study the role of myosin cables at the MEB, we simulated the internalization using a vertex model. Our model predicted that tension at the MEB maintains the interface linearity, prevents cell mixing, and controls the timing of internalization. Consistent with this, pharmacological inhibition of myosin disrupted the MEB, leading to mesectoderm-ectoderm cell mixing and premature internalization. Our model also predicted cell divisions in the ectoderm play a role in maintaining the linearity of the MEB. |
Tuesday, March 15, 2022 3:36PM - 3:48PM |
K05.00004: Symmetry breaking in tissue flow during early Drosophila morphogenesis Emily W 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 live imaging, 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" during morphogenesis. |
Tuesday, March 15, 2022 3:48PM - 4:00PM |
K05.00005: In vivo measurements of embryonal tissue mechanics Behzad Golshaei, Chonglin Guan, An T Pham, Janice M Crawford, Daniel P Kiehart, Christoph F Schmidt Tissue sheet movements are critical in embryonal development. To understand the machinery driving morphogenesis it is important to quantitate the mechanical properties of the involved tissues. We here study the process of dorsal closure (DC) in Drosophila melanogaster embryos. Time-lapse microscopy of the process provides data on the complex tissue movements occurring during DC. In order to elucidate the force generating processes driving the movements, however, one needs to know the tissue material properties. Measuring those properties has been extremely challenging since the embryo is tightly enclosed in an egg shell. We use peeled embryos that are directly accessible to mechanical probing while continuing DC. We apply calibrated twin glass microneedles to directly probe DC tissue response in the living embryos. In addition, we use finite-element modeling (FEM, Comsol) to estimate Young's moduli of the various tissue types involved in DC. We find a modulus of ~700 Pa for amnioserosa tissue, comparable to soft vertebrate tissues. Our novel approach allows us to directly probe tissue mechanics in the developing embryo and it provides the possibility to study the effect that particular molecular players have on material properties and on the forces that drive morphogenesis in embryonal development. |
Tuesday, March 15, 2022 4:00PM - 4:12PM |
K05.00006: Multi-scale mechanical interactions across layers drive folding morphogenesis in the gut Noah P Mitchell, Dillon J Cislo, Suraj Shankar, Yuzheng Lin, Boris I Shraiman, Sebastian J Streichan Understanding how organs transform into their target shapes during development is a challenge at the interface between physics and biology. In visceral organs, multiple tissue layers interact to orchestrate complex shape changes. While there has been significant progress in identifying genetic and anatomical ingredients underlying organogenesis, tracing the dynamics of cell behavior and tissue deformation that drive organ shape change remains an outstanding and essential challenge. Here, leveraging the Drosophila midgut as a model system, we use light-sheet microscopy, genetics, computer vision, and tissue cartography to reconstruct in toto shape dynamics of a developing organ in vivo. We identify the kinematic mechanism driving shape change by linking out-of-plane motion to active contraction patterns. Optogenetic perturbations reveal that muscle activity induces endodermal cell shape change and organ constriction. This induction cascade relies on calcium pulses in the muscle layer that are downstream of hox genes, and calcium inhibition abolishes constrictions. Our multi-scale analysis traces how biology controls a physical process generating whole-organ shape change, offering a kinematic and mechanical mechanism for organogenesis in heterologous tissue layers. |
Tuesday, March 15, 2022 4:12PM - 4:24PM |
K05.00007: Electrical cues regulate hydrostatic pressure and swelling in cysts and organoids Isaac B Breinyn, Gawoon Shim, Daniel J Cohen Lumenization of epithelium is an essential and ubiquitous step across the morphogenic processes needed to produce hollow structures such as alveoli, kidney ducts, and the gut. Once a lumen is established, it undergoes cycles of swelling and relaxation that precede multiple critical developmental events such as branching. Here, we show that electrical cues can drive the swelling of homotypic epithelial cysts and intestinal organoids. This behavior appears to be driven by electrical modulation of key ion channels responsible for chloride ion transport such as CFTR, which we demonstrate through the use of targeted ion channel inhibitors. Interestingly, the level of swelling varies directly with the strength of the electric field, allowing us to program both the rate of growth and the overall size of a spherical cyst or organoid. The rate of swelling is too rapid to implicate cell proliferation, so we hypothesize hyperelastic deformation of the epithelium. To investigate this, we modify a simple energy-minimization model to consider the effect of stimulation on osmotic pressure, hydrostatic pressure, and ion-mediated pumping to predict accelerated cyst swelling. |
Tuesday, March 15, 2022 4:24PM - 4:36PM |
K05.00008: Docking of fire ant rafts using pseudopods Hungtang Ko, Keyana Komilian, Leo Hollingworth, Elliot P Willner, David L Hu Fire ants survive floods by linking their bodies together to build waterproof rafts. This state is precarious, and for the raft to survive, it must eventually dock onto shore for the ants to disembark. In this experimental study, we observe how ant rafts identify potentially docking sites and extend multiple "planks" to simultaneously anchor the raft and release ants ashore. These planks are analogous to pseudopodia, the temporary projections of amoeba. Because the fire ants have poor vision, the direction of each of these planks meanders randomly until it encounters a nearby target. The findings of this study will provide insights into how macroscopic active matter can utilize body deformation and flow as an exploration strategy. |
Tuesday, March 15, 2022 4:36PM - 4:48PM |
K05.00009: Machine learning Drosophila embryogenesis Jonathan Colen, Noah P Mitchell, Nikolas H Claussen, Marion Raich, Sebastian J Streichan, Vincenzo Vitelli Hydrodynamic theories use symmetries and conservation laws to build effective descriptions of many-body systems. This approach can break down in living and active matter, where it is difficult to identify relevant collective variables and the lack of symmetries leaves the functional relationships between variables unconstrained. Such problems arise in embryogenesis, where force-generating motor proteins drive dramatic rearrangements of tissue layers. Here, we show that deep neural networks can learn to map between the time-varying distribution of myosin motors and the cellular flows occurring in developing Drosophila embryos. Our models account for the curved geometry of the embryo and can reconstruct both the cellular flows and myosin configurations with high accuracy at different phases of gastrulation. |
Tuesday, March 15, 2022 4:48PM - 5:00PM |
K05.00010: Sensing the fly embryo's transcription factors Marianne Bauer, Mariela D Petkova, Thomas Gregor, Eric F Wieschaus, William S Bialek Transcription factor (TF) concentrations can be seen as signals that need to be sensed by organisms in order for them to express their genes as precisely as is required during development or during adjustment to different conditions. The low concentration of all the relevant molecules means that these measurements will be noisy, setting the maximum that cells can extract. In embryonic development, as an example, there is a minimum information that the organism needs in order to generate a complex body plan, reproducibly. In the fruit fly embryo, there is evidence that these two information bounds are close to one another, so there is a premium on extracting the most useful or meaningful bits. In previous work we have shown that the information bottleneck provides a natural formulation for this problem. It may thus be possible to view the complex enhancer logic that "reads" the transcription factor concentrations as implementing a solution to an information theoretical optimization problem. Here we explore in more detail what happens when individual enhancers have low information capacity, so that the overall measurement of TF concentrations must be split or shared among multiple elements. Driven by direct measurements of signal and noise in the relevant TFs, we show that these multiple elements must be sensitive to combinations of their inputs, both in abstract and more microscopically realistic models. |
Tuesday, March 15, 2022 5:00PM - 5:12PM |
K05.00011: A spontaneous strain mediated mechanical model of the Drosophila wing disc eversion Abhijeet Krishna, Jana Fuhrmann, Charlie Duclut, Frank Jülicher, Natalie Dye, Carl D Modes Spatially inhomogeneous patterns of local deformations are believed to play an important role in the establishment of global shape change during the development of an embryo. The Drosophila wing imaginal disc is a convenient model system for the study of such patterns and their role in determining shape. A flat epithelial monolayer tissue during the larval stage, the wing imaginal disc grows into a hemispherical dome during pupariation, which then flattens to grow into the wing of the adult fly. This process is known as wing disc eversion. We have analyzed the spatial distribution of individual cell properties, such as apical area, and how these patterns change during eversion. Using a spontaneous strain-mediated mechanical spring lattice model, we test whether the changing spatial distribution of cell properties is enough to explain the emergent shape of wing disc eversion. |
Tuesday, March 15, 2022 5:12PM - 5:24PM |
K05.00012: A mechano-chemical coupling drives fountain streaming and nuclear positioning in Drosophila embryos Claudio Hernandez Lopez, Stefano Di Talia, Alberto Puliafito During early development of the syncytial embryo of Drosophila |
Tuesday, March 15, 2022 5:24PM - 5:36PM |
K05.00013: Cellular Compartmentalisation and Receptor Promiscuity as a strategy for accuracy and robustness in Positional Inference during Morphogenesis Krishnan S Iyer, Chaitra Prabhakara, Madan Rao, Satyajit Mayor Precise spatial patterning of cell fate during morphogenesis requires accurate inference of cellular position. In making such inferences from morphogen profiles, cells must contend with inherent stochasticity in morphogen production, transport, sensing and signalling. Using multiple signalling mechanisms in development as motivation, we show how cells may utilise multiple tiers of processing (compartmentalisation) and parallel branches (multiple receptor types), together with feedback control, to bring about fidelity in morphogenetic decoding of their positions within a developing tissue. By simultaneously deploying specific and nonspecific receptors, cells achieve a more robust inference. This distributed information processing at the scale of the cell highlights how local cell autonomous control facilitates global tissue scale design. |
Tuesday, March 15, 2022 5:36PM - 5:48PM |
K05.00014: Modeling helical shape formation in bacteria Luyi Qiu, Cesar L Pastrana, Ulrich Gerland, Shahaf Armon, Ariel Amir Many bacterial species are helical in form, including the widespread pathogen H. pylori. Motivated by recent experiments on H. pylori showing that cell wall synthesis is not uniform, we investigate the possible mechanism of helix formation induced by elastic heterogeneity. We show, experimentally and theoretically, that helical morphogenesis can be produced by pressurizing an elastic cylindrical vessel with helical reinforced lines. The properties of the pressurized helix highly depend on the initial helical angle of the reinforced region. We find that steep angles may result in crooked helices with reduced end to end distance upon pressurization. This provides a possible mechanism for active shape transformations due to local osmolarity changes and may also inspire the design of novel pressure-controlled helical actuators. |
Tuesday, March 15, 2022 5:48PM - 6:00PM |
K05.00015: Inferring the Stochastic Dynamics of Bacterial Growth and Shape Fluctuations Kurt C Cylke, Shiladitya Banerjee Growing rod-shaped bacterial cells exhibit stochastic shape dynamics but the nature of noise and fluctuations remains poorly understood. A quantitative understanding of the noise in bacterial growth and how it changes under different nutrient conditions would provide better insight into cell-to-cell variability and intergenerational fluctuations. Using multigenerational growth and shape data on single Escherichia coli cells, we derive the equations for cell growth and morphodynamics. Interestingly, we find that E. coli cells elongate faster than an exponential within an individual generation. We propose a physical model that explains this phenomenon based on heterogeneous patterning of cell growth. Using this new model and statistical inference on large datasets, we construct the Langevin equations for the shape dynamics of E. coli cells in different growth conditions. We then use the model to make predictions about bacterial adaptation to nutrient shifts, resulting in a simulation that accurately represents noise and fluctuations in cell shape in non-steady growth conditions. |
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