The Selector Gene apterous and Notch Are Required to Locally Increase Mechanical Cell Bond Tension at the Drosophila Dorsoventral Compartment Boundary.

Marcus Michel,Katrin Rudolf,Frank Jülicher,Christian Dahmann,Lisa Bialas,Maryam Aliee,Amit Singh

doi:10.1371/journal.pone.0161668

Marcus Michel, Katrin Rudolf + Show 5 more

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https://doi.org/10.1371/journal.pone.0161668

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Abstract

The separation of cells with distinct fates and functions is important for tissue and organ formation during animal development. Regions of different fates within tissues are often separated from another along straight boundaries. These compartment boundaries play a crucial role in tissue patterning and growth by stably positioning organizers. In Drosophila, the wing imaginal disc is subdivided into a dorsal and a ventral compartment. Cells of the dorsal, but not ventral, compartment express the selector gene apterous. Apterous expression sets in motion a gene regulatory cascade that leads to the activation of Notch signaling in a few cell rows on either side of the dorsoventral compartment boundary. Both Notch and apterous mutant clones disturb the separation of dorsal and ventral cells. Maintenance of the straight shape of the dorsoventral boundary involves a local increase in mechanical tension at cell bonds along the boundary. The mechanisms by which cell bond tension is locally increased however remain unknown. Here we use a combination of laser ablation of cell bonds, quantitative image analysis, and genetic mutants to show that Notch and Apterous are required to increase cell bond tension along the dorsoventral compartment boundary. Moreover, clonal expression of the Apterous target gene capricious results in cell separation and increased cell bond tension at the clone borders. Finally, using a vertex model to simulate tissue growth, we find that an increase in cell bond tension at the borders of cell clones, but not throughout the cell clone, can lead to cell separation. We conclude that Apterous and Notch maintain the characteristic straight shape of the dorsoventral compartment boundary by locally increasing cell bond tension.

Highlights

The specification of cell fate is important for organizing cells into functional tissues during animal development
We have previously shown that two physical mechanisms can account for the shape of the dorsoventral compartment boundary (DV) boundary: First, global tension anisotropies in the wing imaginal disc that result in cell elongation and oriented cell division and, second, a local increase in mechanical tension at adherens junctions along the compartment boundary [28]
Adherens junctions were identified by E-cadherin immunostainings and the DV boundary was visualized by expression of GFP under control of apGal4

Summary

Introduction

The specification of cell fate is important for organizing cells into functional tissues during animal development. The anteroposterior compartment boundary (AP boundary) is established during embryonic development and separates cells of anterior and posterior fates in the wing primordium [7]. During mid-third instar larval development, for example, Apterous induces expression of the two leucine-rich repeat proteins Capricious and Tartan that have been proposed to be involved in maintaining the straight shape of the DV boundary [24]. Apterous induces expression of Fringe, a glycosyltransferase that modifies several EGF domains in the extracellular region of the Notch receptor [25,26]. Notch signal transduction in cells along the DV boundary induces expression of Wingless, which in turn contributes to wing disc patterning and growth [27]. Clones of cells mutant for apterous or Notch disturb the shape of the DV boundary [17,18], showing that Apterous and Notch play important roles in separating dorsal and ventral cells along this compartment boundary

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