Emergence of a geometric pattern of cell fates from tissue-scale mechanics in the Drosophila eye

Abstract

Pattern formation of biological structures involves the arrangement of different types of cells in an ordered spatial configuration. In this study, we investigate the mechanism of patterning the Drosophila eye epithelium into a precise triangular grid of photoreceptor clusters called ommatidia. Previous studies had led to a long-standing biochemical model whereby a reaction-diffusion process is templated by recently formed ommatidia to propagate a molecular prepattern across the eye. Here, we find that the templating mechanism is instead, mechanochemical in origin; newly born columns of differentiating ommatidia serve as a template to spatially pattern flows that move epithelial cells into position to form each new column of ommatidia. Cell flow is generated by a source and sink, corresponding to narrow zones of cell dilation and contraction respectively, that straddle the growing wavefront of ommatidia. The newly formed lattice grid of ommatidia cells are immobile, deflecting and focusing the flow of other cells. Thus, the self-organization of a regular pattern of cell fates in an epithelium is mechanically driven.

Patterning of the Drosophila retina by the morphogenetic furrow

“…A recent study by Richard Carthew’s group describes a breakthrough in developing a long-term ex vivo culturing system for the eye-antennal disc. It uses a unique culture media as well as cutting-edge time-lapse microscopy and image analysis to visualize the birth and development of approximately four to five columns of ommatidia over the course of 10–12 h ( Gallagher et al, 2022 ). Their ex vivo system is an excellent proxy for studying in vivo eye development because all aspects of gene expression, tissue growth, cell fate specification, and planar cell polarity appear to be recapitulated.…”

3D Organisation of Cells in Pseudostratified Epithelia

“…Even the hexagonal ommatidia in the Drosophila eye are each composed of 21 differently-sized apical cell areas, which are predominantly not hexagonal [48]. The arrangement into hexagonal ommatidia relies on the careful adjustment of cell adhesion, cortical tension, and cell dilation [49][50][51]. As mixed cross-sectional cell areas are most favourable, epithelial cells easily disperse from a clone with smaller cells, while they remain clustered without such a cell size difference relative to the surrounding tissue, potentially facilitating the spreading of tumour cells [16].…”

TubULAR: Tracking in toto deformations of dynamic tissues via constrained maps

“…In a particularly fruitful methodological advance, the community has applied differential geometry techniques to establish 'tissue cartography' methods for mapping curved tissues to a planar representation, dramatically reducing the computational power required to track and store 3D data [29][30][31]. This framework has facilitated insights in a wide variety of systems including fly wings [32], eyes [33], and egg chambers [34], ascidian vasculature [35], zebrafish hearts [30] and endoderm [29], and mouse intestines [36]. By building on this theme, we implement automated methods for registering dynamic surfaces across time and classifying the signatures of tissue deformation.…”

“…In a particularly fruitful methodological advance, the community has applied 'tissue cartography' methods that map curved tissues to a planar representation, dramatically reducing the computational power required to store and analyze 3D data [23][24][25][26]. This advance has facilitated insights in a wide variety of systems including fly wings [27], eyes [28], egg chambers [29], ascidian vasculature [30], zebrafish endoderm [23], and mouse intestines [31].…”