Pattern formation in the Drosophila eye

Abstract

The insect compound eye is one of the most precise and highly ordered patterns in the living world. It develops from an unpatterned simple epithelium by a series of cell fate decisions and complex morphogenetic movements. In the first days of metamorphosis, this interplay is particularly noticeable. Recent insights have revealed how interactions between neighboring cells drive the process. Interaction between Delta on cone cells and Notch proteins on the surface of their neighbors induces the first pigment cells to differentiate. The primary pigment cells then express a Nephrin protein, Hibris, that interacts with a different Nephrin, Roughest, on their neighbors. Heterophilic adhesion between Hibris and Roughest results in remodeling contacts between cells to favor their contact with the pigment cells. In conjunction, the primary pigment cells signal to their neighbors through the EGF receptor to survive, rather than undergo apoptosis. This sorting and culling process results in a sculpted pattern with a precise number and position of cells that is repeated hundreds of times in each compound eye.

Figure 1. Pattern formation in the pupal eye

The apical surface of eyes at different stages of pupal life. Grey cells are uncommitted IPCs and coloured cells are determined. (A) At the beginning of pupation, the cone cells (blue and yellow) are embedded within a mosaic of IPCs. (B) After 20 hours pupation, PP cells (orange) are enlarging and surrounding the cone cells. (C) After 30 hours pupation, PP cells are contacting each other. (D) After 40 hours pupation, cone and PP cells are enlarging, and IPCs sort into single rows between them. IPCs positioned in certain niches differentiate into SP (green) and TP cells (red). IPCs which are not committed undergo apoptosis. (E) After 60 hours pupation, pattern formation is complete. Figure is modified after [2].

Figure 2. Cell topologies and geometries in the eye

(A,B) Schematic ommatidium at 60 hours of pupal life. A cross-section view (A) is at the level of the adherens junction (AJ), and a side view (B) is equatorial to the midplane. A central group of cone cells are laterally surrounded by the two PP cells. The cone cell group sits over a cluster of eight photoreceptor cells (R) and under the lens (L). A lattice of SP and TP cells, and bristles are indicated. Nuclei in their defined positions are indicated as ovals. The schematics do not contain the small apical and basal processes of photoreceptor and cone cells that project from top to bottom. (C) Cell outlines of a retina at 55 hours of pupal life, as stained for DE-cadherin (green) and DN-cadherin (red). Colocalization of the cadherins results in orange staining.

Figure 3. IPC Sorting and Apoptosis

IPCs are marked in beige, and PPs and cone cells are marked in blue. Roughest protein is indicated by brown lines in IPCs while Hibris protein is indicated by green lines in cones and PPs. (A) At 10 hours pupal life, low uniform levels of Roughest in IPCs result in uniform contact between cells. (B) At 30 hours pupal life, heterophilic interaction between Hibris and Roughest (thick green and brown lines) along IPC:PP contacts result in sorting such that the size of IPC:IPC contacts is reduced in favour of IPC:PP contacts. (C) One IPC establishes contact with a third PP and becomes (D) a TP cell. The other two competing IPCs then must compete for a SP cell fate. Some IPCs which fail to outcompete undergo apoptosis (circles). Figure is modeled after [12].