Drosophila Retinal Patterning

Abstract

The Drosophila eye is an outstanding model system for exploring fundamental mechanisms of growth and development. The adult eye is composed of a perfect hexagonal lattice of ∼750 unit eyes, or ommatidia, each containing precisely 20 well‐characterized cells. The eye develops from the eye/antennal imaginal disc, a flattened epithelial sac. During larval and pupal development, cells in the disc grow and undergo compartmentalisation, cell cycle arrest, differentiation, directed movement, and apoptosis, all utilising gene networks and signalling pathways similar to those in vertebrates. The genetic accessibility of Drosophila, together with the precision of eye development, makes the fly retina an extremely useful system with which to investigate the roles of genes and signalling pathways in development.

Key Concepts

  • Adult Drosophila eyes contain ∼750 ommatidia, or unit eyes; each ommatidium is made up of precisely 20 cells, each of which can be identified by its position and protein expression.
  • Like other adult structures in Drosophila, the eye develops from an imaginal disc, a flattened sac of epithelial cells that develops during larval and pupal stages.
  • Drosophila retinal development utilises gene regulatory networks similar to those in human eye development.
  • Photoreceptor differentiation requires passage of the morphogenetic furrow, an invagination in eye disc that moves across the tissue from posterior to anterior during larval development.
  • Photoreceptors differentiate during larval stages using signals emanating from previously differentiated cells, rather than through lineage restrictions.
  • During pupal development, accessory cells differentiate and apoptosis reduces the number of cells in each ommatidium to 20.
  • Cell interactions during pupal development produce the precise hexagonal lattice characteristic of the adult Drosophila eye.

Keywords: retina; development; Drosophila; photoreceptor; patterning; eye

Figure 1. (a) The eye/antennal imaginal disc develops into structures in the adult head. Left, a side view of the disc showing the peripodial epithelium (yellow) overlying the eye disc underneath (red). Middle, a top‐down view of the disc, showing regions that will develop into the eye, ocelli, maxillary palps, antenna and cuticle. Right, structures of the adult eye. (b) section of the adult eye shows rhabdomeres in individual ommatidia; photoreceptors are labelled. Note the mirror image arrangement of the rhabdomeres above and below the equator (dashed line). (c) scanning electron micrograph of the adult eye. (d) Side view schematic of cell arrangement in an adult ommatidium. Posterior is to the left in all figures.
Figure 2. (a) Schematic of gene expression in the eye/antennal disc through larval development and the stepwise differentiation of the photoreceptor cells. Note that ommatidial clusters rotate as they mature and that they are mirror images above and below the equator (dashed line). (b) view of a third instar eye disc stained with antibodies against DE‐Cadherin (green) and the cell adhesion protein Echinoid (red). DE‐Cadherin outlines the small apical profiles of cells in the morphogenetic furrow (MF). As cells emerge from the furrow (left), DE‐cadherin is highest on the membranes of cells in the ommatidial precluster. Slightly later (next row to the left), it is most visible on the membranes of R8, R2, and R5. (c) Schematic of gradients influencing R3 and R4 differentiation and ommatidial rotation. Wg is secreted from the edges of the disc; Fz activity is highest in cells closest to the equator. Higher Fz activity leads to expression of Dl, which activates N on the neighbouring cell, leading to R3 and R4 specification. Photoreceptors in (c) are arranged as they would be below the equator.
Figure 3. Pupal Development. (a) Small region of the eye at 40 h APF. The outlines of cells are visualised via detection of adherens junctions (in green).Source: From Johnson, RI. . Adhesion and the Cytoskeleton in the Drosophila Pupal Eye. In Molecular Genetics of Axial Patterning, Growth and Disease in the Drosophila Eye. A. Singh and M. Kango‐Singh, editors. Springer, Cham. 189–213 (b) The eye at 22 h APF, marked by a gradient of development so that step‐wise changes in cell morphologies can be seen, as indicated. Cells have been colour‐coded as per key.Source: Adapted from (Hellerman et al., ). (c) Increased apoptosis of interommatidial cells or (d) decreased apoptosis still leads to mainly hexagonal ommatidia by 40 h APF.
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Spencer, Susan A, Johnson, Ruth I, and Setu, Bipul(Dec 2020) Drosophila Retinal Patterning. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0029229]