Emergence of a geometric pattern of cell fates from tissue-scale mechanics in the Drosophila eye
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Evaluation Summary:
This paper will have a high impact for all developmental and cell biologists who are interested in tissue patterning and organogenesis. It provides unexpected insights into the problem of regular spacing of sub-organ structures. The study is based on innovative live imaging technology with state of the art analysis tools.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript.)
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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.
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Evaluation Summary:
This paper will have a high impact for all developmental and cell biologists who are interested in tissue patterning and organogenesis. It provides unexpected insights into the problem of regular spacing of sub-organ structures. The study is based on innovative live imaging technology with state of the art analysis tools.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript.)
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Reviewer #1 (Public Review):
This paper by Gallagher et al (Carthew lab with M. Mani) addresses how the regular patterning of ommatidial preclusters emerges from the morphogenetic furrow (MF) during eye development in Drosophila. The study uses a novel live imaging protocol that allows the visualization of cell movements and associated contractions and dilations as the MF moves from posterior to anterior across the eye discs and leaves the evenly spaced preclusters in its wake. The highly regularly spaced ommatidia, compose of photoreceptors, has served as a paradigm for many studies involving cell signaling pathways, lateral inhibition, and a reaction-diffusion model has been proposed to be at the center of the even spaced out ommatidia. Here the authors show a very unexpected discovery that the regular spacing is generated by a …
Reviewer #1 (Public Review):
This paper by Gallagher et al (Carthew lab with M. Mani) addresses how the regular patterning of ommatidial preclusters emerges from the morphogenetic furrow (MF) during eye development in Drosophila. The study uses a novel live imaging protocol that allows the visualization of cell movements and associated contractions and dilations as the MF moves from posterior to anterior across the eye discs and leaves the evenly spaced preclusters in its wake. The highly regularly spaced ommatidia, compose of photoreceptors, has served as a paradigm for many studies involving cell signaling pathways, lateral inhibition, and a reaction-diffusion model has been proposed to be at the center of the even spaced out ommatidia. Here the authors show a very unexpected discovery that the regular spacing is generated by a mechanical mechanism, generated by evenly spaced region of cell flow. It is proposed that the cell flow is generated by a pressure gradient, which is caused by a zone of cellular dilation posterior to the MF, and the existing "template" of spaced R8-centerd preclusters. It is further shown that the spacing indeed depends on the anterior "template" and that this is depending on the role of the Scabrous gene.
This is overall an exciting paper and it will make an excellent contribution to the field and developmental patterning in general.
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Reviewer #2 (Public Review):
This is an impressive study, that characterizes, for the first time, the dynamic cell behavior in the differentiating eye imaginal disc, that was hitherto believed to be static. The cell movements that are uncovered are not uniform or random, but rather correspond to, and perhaps dictate, the regular spacing of photoreceptor clusters. The identification and characterization of these cell movements is clearly valuable and should be considered in future analyses of cell differentiation in this tissue.
The major claim of the paper is that this patterned cell movement is sufficient to generate the regular spacing in the developing eye, by separating clusters of Atonal-expressing cells. The suggestion is that the signaling pathways that were identified over decades of work are executing the determination that was …
Reviewer #2 (Public Review):
This is an impressive study, that characterizes, for the first time, the dynamic cell behavior in the differentiating eye imaginal disc, that was hitherto believed to be static. The cell movements that are uncovered are not uniform or random, but rather correspond to, and perhaps dictate, the regular spacing of photoreceptor clusters. The identification and characterization of these cell movements is clearly valuable and should be considered in future analyses of cell differentiation in this tissue.
The major claim of the paper is that this patterned cell movement is sufficient to generate the regular spacing in the developing eye, by separating clusters of Atonal-expressing cells. The suggestion is that the signaling pathways that were identified over decades of work are executing the determination that was initially triggered by cell movement. Therefore, a critical review of the paper should examine if this provocative claim is indeed substantiated by the results.
We believe that the causal role of cell movement has not been conclusively demonstrated. While the study is novel and will have a broad impact on future studies, the claims regarding the causal role of cell movement in dictating ommatidial spacing cannot be made until critical experiments will be carried out.
In conclusion, this paper examines, for the first time, the movement of cells within the differentiating eye disc. The patterns of movement identified are highly correlated to the emerging pattern of photoreceptor clusters. Therefore, they will certainly have to be taken into account in future analyses of this system. The current data cannot distinguish between cause and consequence vis a vis the role of cell movements in photoreceptor spacing. The data is of high quality, however, the conclusions need to be toned down. -
