Abstract

Regulation of cell growth and cell division plays fundamental roles in tissue morphogenesis. However, the mechanisms of regulating tissue elongation through cell growth and cell division are still not well understood. The wing imaginal disc of Drosophila provides a model system that has been widely used to study tissue morphogenesis. Here we use a recently developed two-dimensional cellular model to study the mechanisms of regulating tissue elongation in Drosophila wing. We simulate the effects of directional cues on tissue elongation. We also computationally analyze the role of reduced cell size. Our simulation results indicate that oriented cell divisions, oriented mechanical forces, and reduced cell size can all mediate tissue elongation, but they function differently. We show that oriented cell divisions and oriented mechanical forces act as directional cues during tissue elongation. Between these two directional cues, oriented mechanical forces have a stronger influence than oriented cell divisions. In addition, we raise the novel hypothesis that reduced cell size may significantly promote tissue elongation. We find that reduced cell size alone cannot drive tissue elongation. However, when combined with directional cues, such as oriented cell divisions or oriented mechanical forces, reduced cell size can significantly enhance tissue elongation in Drosophila wing. Furthermore, our simulation results suggest that reduced cell size has a short-term effect on cell topology by decreasing the frequency of hexagonal cells, which is consistent with experimental observations. Our simulation results suggest that cell divisions without cell growth play essential roles in tissue elongation.

Highlights

  • Regulation of cell growth and cell division plays fundamental roles in tissue morphogenesis [1,2,3,4]

  • We find that reduced cell size alone cannot drive tissue elongation, as it does not have directional information

  • We first computationally studied the effect of oriented cell divisions (OCD) with our cellular model to mimic the pupal development between 15 and 24 hour after puparium formation in Drosophila wing, without considering the effects of reduced cell size and oriented mechanical forces

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Summary

Introduction

Regulation of cell growth and cell division plays fundamental roles in tissue morphogenesis [1,2,3,4]. Cells in the wing imaginal disc proliferate, forming an elongated tissue shape along its proximal-distal (PD) axis [3,17,18]. Dachs is a molecule known to mediate the orientation of cell divisions in the developing Drosophila wing [18]. Theoretical studies suggest that Dachs may indirectly orient the mitotic spindle as a result of the elongated cell shape due to the polarized apical cell junctions [18]. In addition to Dachs, microtubules are another class of molecules that influence the orientation of mitotic spindles during cell divisions [24,25,26,27]. The orientation of cell divisions is less focused along the PD-axis in ds mutants than in wild-type [17]

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