Patterned Anchorage to the Apical Extracellular Matrix Defines Tissue Shape in the Developing Appendages of Drosophila

How tissues acquire their characteristic shape is a fundamental unresolved question in biology. While genes have been characterized that control local mechanical forces to elongate epithelial tissues, genes controlling global forces in epithelia have yet to be identified. Here, we describe a genetic pathway that shapes appendages in Drosophila by defining the pattern of global tensile forces in the tissue. In the appendages, shape arises from tension generated by cell constriction and localized anchorage of the epithelium to the cuticle via the apical extracellular-matrix protein Dumpy (Dp). Altering Dp expression in the developing wing results in predictable changes in wing shape that can be simulated by a computational model that incorporates only tissue contraction and localized anchorage. Three other wing shape genes, narrow, tapered, and lanceolate, encode components of a pathway that modulates Dp distribution in the wing to refine the global force pattern and thus wing shape.Peer reviewe

Raw data: Patterned apoptosis has an instructive role for local growth and tissue shape regulation in a fast-growing epithelium

<p>What regulates organ size and shape remains one fundamental mystery of modern biology. Research in this area has primarily focused on deciphering the regulation in time and space of growth and cell division, while the contribution of cell death has been overall neglected. This includes studies of the <i>Drosophila</i> wing, one of the best characterised systems for the study of growth and patterning, undergoing massive growth during larval stage and important morphogenetic remodeling during pupal stage. So far, it has been assumed that cell death was relatively neglectable in this tissue both during larval and pupal stage and as a result the pattern of growth was usually attributed to the distribution of cell division. Here, using systematic mapping and registration combined with quantitative assessment of clone size and disappearance as well as live imaging, we outline a persistent pattern of cell death and clone elimination emerging in the larval wing disc and persisting during pupal wing morphogenesis. Local variation of cell death is associated with local variation of clone size, pointing to an impact of cell death on local growth which is not fully compensated by proliferation. Using morphometric analyses of adult wing shape and genetic perturbations, we provide evidence that patterned death affects locally and globally adult wing shape and size. This study describes a roadmap for precise assessment of the contribution of cell death to tissue shape, and outlines an important instructive role of cell death in modulating quantitatively local growth and morphogenesis of a fast-growing tissue.</p><p>This repository contains the raw data (local projection images, ROI and quantificatiosn) of the Current Biology article "<strong>Patterned apoptosis has an instructive role for local growth and tissue shape regulation in a fast-growing epithelium".</strong></p&gt

Multiple Influences of Mechanical Forces on Cell Competition

International audienceCell competition is a widespread process leading to the expansion of one cell population through the elimination and replacement of another. A large number of genetic alterations can lead to either competitive elimination of the mutated population or expansion of the mutated cells through the elimination of the neighbouring cells. Several processes have been proposed to participate in the preferential elimination of one cell population, including competition for limiting extracellular pro-survival factors, communication through direct cell–cell contact, or differential sensitivity to mechanical stress. Recent quantitative studies of cell competition have also demonstrated the strong impact of the shape of the interfaces between the two populations. Here, we discuss the direct and indirect contribution of mechanical cues to cell competition, where they act either as modulators of competitive interactions or as direct drivers of cell elimination. We first discuss how mechanics can regulate contact-dependent and diffusion-based competition by modulating the shape of the interface between the two populations. We then describe the direct contribution of mechanical stress to cell elimination and competition for space. Finally, we discuss how mechanical feedback also influences compensatory growth and triggers preferential expansion of one population

Microtubule disassembly by caspases is the rate-limiting step of cell extrusion

Posté sur BioRxiv le 15 octobre 2021Abstract Epithelial cell death is essential for tissue homeostasis, robustness and morphogenesis. The expulsion of epithelial cells following caspase activation requires well-orchestrated remodeling steps leading to cell elimination without impairing tissue sealing. While numerous studies have provided insight about the process of cell extrusion, we still know very little about the relationship between caspase activation and the remodeling steps of cell extrusion. Moreover, most studies of cell extrusion focused on the regulation of actomyosin and steps leading to the formation of a supracellular contractile ring. However, the contribution of other cellular factors to cell extrusion has been poorly explored. Using the Drosophila pupal notum, a single layer epithelium where most extrusion events are caspase-dependent, we first showed that the initiation of cell extrusion and apical constriction are surprisingly not associated with the modulation of actomyosin concentration/dynamics. Instead, cell apical constriction is initiated by the disassembly of a medio-apical mesh of microtubules which is driven by effector caspases. We confirmed that local and rapid increase/decrease of microtubules is sufficient to respectively expand/constrict cell apical area. Importantly, the depletion of microtubules is sufficient to bypass the requirement of caspases for cell extrusion. This study shows that microtubules disassembly by caspases is a key rate-limiting steps of extrusion, and outlines a more general function of microtubules in epithelial cell shape stabilisation

Microtubule disassembly by caspases is an important rate-limiting step of cell extrusion

International audienceThe expulsion of dying epithelial cells requires well-orchestrated remodelling steps to maintain tissue sealing. This process, named cell extrusion, has been mostly analysed through the study of actomyosin regulation. Yet, the mechanistic relationship between caspase activation and cell extrusion is still poorly understood. Using the Drosophila pupal notum, a single layer epithelium where extrusions are caspase-dependent, we showed that the initiation of cell extrusion and apical constriction are surprisingly not associated with the modulation of actomyosin concentration and dynamics. Instead, cell apical constriction is initiated by the disassembly of a medio-apical mesh of microtubules which is driven by effector caspases. Importantly, the depletion of microtubules is sufficient to bypass the requirement of caspases for cell extrusion, while microtubule stabilisation strongly impairs cell extrusion. This study shows that microtubules disassembly by caspases is a key rate-limiting step of extrusion, and outlines a more general function of microtubules in epithelial cell shape stabilisation

Quantitative Morphological Variation in the Developing Drosophila Wing

Quantitative genetic variation in morphology is pervasive in all species and is the basis for the evolution of differences among species. The measurement of morphological form in adults is now beginning to be combined with comparable measurements of form during development. Here we compare the shape of the developing wing to its adult form in a holometabolous insect, Drosophila melanogaster. We used protein expression patterns to measure shape in the developing precursors of the final adult wing. Three developmental stages were studied: late larval third instar, post-pupariation and in the adult fly. We studied wild-type animals in addition to mutants of two genes (shf and ds) that have known effects on adult wing shape and size. Despite experimental noise related to the difficulty of comparing developing structures, we found consistent differences in wing shape and size at each developmental stage between genotypes. Quantitative comparisons of variation arising at different developmental stages with the variation in the final structure enable us to determine when variation arises, and to generate hypotheses about the causes of that variation. In addition we provide linear rules allowing us to link wing morphology in the larva, with wing morphology in the pupa. Our approach provides a framework to analyze quantitative morphological variation in the developing fly wing. This framework should help to characterize the natural variation of the larval and pupal wing shape, and to measure the contribution of the processes occurring during these developmental stages to the natural variation in adult wing morphology.Peer reviewe

Patterned apoptosis has an instructive role for local growth and tissue shape regulation in a fast-growing epithelium

International audienceWhat regulates organ size and shape remains one fundamental mystery of modern biology. Research in this area has primarily focused on deciphering the regulation in time and space of growth and cell division, while the contribution of cell death has been overall neglected. This includes studies of the Drosophila wing, one of the best-characterized systems for the study of growth and patterning, undergoing massive growth during larval stage and important morphogenetic remodeling during pupal stage. So far, it has been assumed that cell death was relatively neglectable in this tissue both during larval stage and pupal stage, and as a result, the pattern of growth was usually attributed to the distribution of cell division. Here, using systematic mapping and registration combined with quantitative assessment of clone size and disappearance as well as live imaging, we outline a persistent pattern of cell death and clone elimination emerging in the larval wing disc and persisting during pupal wing morphogenesis. Local variation of cell death is associated with local variation of clone size, pointing to an impact of cell death on local growth that is not fully compensated by proliferation. Using morphometric analyses of adult wing shape and genetic perturbations, we provide evidence that patterned death locally and globally affects adult wing shape and size. This study describes a roadmap for precise assessment of the contribution of cell death to tissue shape and outlines an important instructive role of cell death in modulating quantitatively local growth and morphogenesis of a fast-growing tissue

Aperture number influences pollen survival in Arabidopsis mutants

International audiencePREMISE OF THE STUDY: Pollen grains are subject to intense dehydration before dispersal. They rehydrate after landing on a stigma or when placed in humid environment by absorbing water from the stigma or surroundings. Resulting fluctuations in water content cause pollen grains to undergo significant changes in volume. Thus, morphological or structural adaptations might exist to help pollen adjust to sudden volume changes, though little is known about the correlation between pollen morphology and its ability to accommodate volume changes. We studied the effect of one morphological feature of pollen grains, the aperture number, on pollen wall resistance to water inflow in Arabidopsis thaliana.METHODS: We used three Arabidopsis thaliana mutants that differ in the number of apertures in their pollen (zero, four, or a mix of four to eight, respectively) and the wild type with pollen with three apertures. We tested pollen survival in solutions with various mannitol concentrations.KEY RESULTS: The number of intact pollen grains increased with increasing mannitol concentration for all pollen morphs tested. At a given mannitol concentration, however, an increase in aperture number was associated with an increase in pollen breakage.CONCLUSIONS: Aperture patterns, i.e., number, shape, and position, influence the capacity to accommodate volume variations in pollen grains. When subjected to water inflow, pollen grains with few apertures survive better than pollen with many apertures. Trade-offs between survival and germination are likely to be involved in the evolution of pollen morphology

Field collections reveal that São Tomé is the Afrotropical island with the highest diversity of drosophilid flies (Diptera: Drosophilidae)

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