Hexagonal patterning of the Drosophila eye

Abstract

A complex network of transcription factor interactions propagates across the larval eye disc to establish columns of evenly-spaced R8 precursor cells, the founding cells of Drosophila ommatidia. After the recruitment of additional photoreceptors to each ommatidium, the surrounding cells are organized into their stereotypical pattern during pupal development. These support cells - comprised of pigment and cone cells - are patterned to encapsulate the photoreceptors and separate ommatidia with an hexagonal honeycomb lattice. Since the proteins and processes essential for correct eye patterning are conserved, elucidating how these function and change during Drosophila eye patterning can substantially advance our understanding of transcription factor and signaling networks, cytoskeletal structures, adhesion complexes, and the biophysical properties of complex tissues during their morphogenesis. Our understanding of many of these aspects of Drosophila eye patterning is largely descriptive. Many important questions, especially relating to the regulation and integration of cellular events, remain.

Keywords: Drosophila eye; Interommatidial cells; Morphogenesis; Ommatidia; Pigment cells; R8.

Figure 1:. The Drosophila compound eye is highly ordered.

(A) Small region of the pupal eye at 40 h APF. AJs have been detected with antibodies to E-Cadherin. The epithelial support cells are color-coded, as indicated. (B) Small region of a scanning electron micrograph of the adult eye. A single ommatidium is illustrated to emphasize the cells that lie below the rounded lenses, although in the adult eye the IC lattice is more compressed than illustrated. (Images: RIJ)

Figure 2:. Patterning begins in the larval eye with selection of the R8-precursors.

(A) A third instar larval eye disc, with photoreceptors detected with anti-Elav (red) and dividing cells detected with anti-phospho-histone 3B. The MF is indicated with a bracket as it proceeds from posterior (right) to anterior (left). (Image: RIJ) (B) Small region of the eye disc, at higher magnification than the image in A., with Ato detection (Image: Susan Spencer) (C) Cartoon of ato expression. Cell outlines do not accurately reflect the shapes of cells in the larval disc. (D) The network of major signals and interactions that regulate ato expression. Light green indicates interactions that regulate the ato band; medium and dark green represents Ato in the IGs and R8 precursors. (E) Graphical summary of R8 selection as the MF moves from posterior, as per models/computer simulations. (Drawings: RIJ, inspired by (Courcoubetis et al., 2019; Lubensky et al., 2011)).

Figure 3:. Local cell movements, growth and shape changes characterize the early pupal eye.

(A) Central region of the pupal eye at 22 h APF, which is marked by a gradient of development evident for another ~8 h. Examples of intercalating ICs are marked in green, cone cells in orange and encircling 1° cells in yellow. Three ICs that will compete for a single 3° niche are in blue. Posterior is to the right. (Image adapted from (Hellerman et al., 2015). (B) Model of the molecular regulation of intercalation. See text for details and note that model requires experimental confirmation. (C) At right, Rst (red) and E-cad (green) in ommatidia and, in panels below, at higher magnification in ICs. Rst becomes excluded from IC-IC boundaries and concentrated at 1°-IC where it complexes with Hbs (not shown) (Image adapted from (Johnson et al., 2012). At left, live-imaging of MyoII (red) and actin (green) in ICs. Bracket indicates contraction and expansion of the 2°−3° junction; arrowheads reflect associated MyoII and F-actin accumulation. (Image adapted from (Del Signore et al., 2018). Below, model of dynamic cytoskeletal and junction events that drive reshaping of the ICs. See text for details.

Figure 4:. Junction and cytoskeletal factors drive shaping of cone and 1° cells.

(A) Single ommatidia, with cone cells in orange and the outlines of 1° cells in yellow. Images are presented to scale. (Adapted from (Johnson, 2020)). (B) Illustration of the T1-T2-T3 transition of cone cells with factors that drive intercalation and the acquisition of the final CC shapes and (C) illustration of the factors that influence the final 1° shapes. See text for details. Note experimental confirmation of the models presented is incomplete.