Semper's cells in the insect compound eye: Insights into ocular form and function

Abstract

The arthropod compound eye represents one of two major eye types in the animal kingdom and has served as an essential experimental paradigm for defining fundamental mechanisms underlying sensory organ formation, function, and maintenance. One of the most distinguishing features of the compound eye is the highly regular array of lens facets that define individual eye (ommatidial) units. These lens facets are produced by a deeply conserved quartet of cuticle-secreting cells, called Semper cells (SCs). Also widely known as cone cells, SCs were originally identified for their secretion of the dioptric system, i.e. the corneal lens and underlying crystalline cones. Additionally, SCs are now known to execute a diversity of patterning and glial functions in compound eye development and maintenance. Here, we present an integrated account of our current knowledge of SC multifunctionality in the Drosophila compound eye, highlighting emerging gene regulatory modules that may drive the diverse roles for these cells. Drawing comparisons with other deeply conserved retinal glia in the vertebrate single lens eye, this discussion speaks to glial cell origins and opens new avenues for understanding sensory system support programs.

Keywords: Animal vision; Crystalline cone; Eye evolution; Glia; IRM proteins; Lens; Müller glia; Pax2; PaxB; Prospero; Prox1; SoxB.

Figure 1:. Structural comparison of arthropod compound eye and vertebrate single lens eye.

SC/MG represents radial glia-like support cells, Semper cells (SCs) in arthropod eyes and Müller glia (MG) in vertebrate eyes. RPE = retinal pigment epithelium.

Figure 2:. Cellular events during Drosophila late larval eye development.

Green = retinal neurons (photoreceptors), dark blue = anterior (A) and posterior (P) Semper cells (SCs), light blue = equatorial (Eq) and Polar (Pl) SCs. MF = morphogenetic furrow, a moving front that stops progenitor cell proliferation in G1 and initiates a first wave of neurogenesis of 5 neurons/ommatidia (PRs R8, 2/5 and 3/4). An additional round of proliferation at the second mitotic wave (SMW) provides sufficient progenitors for building the remainder of the eye. Key transcription factors are listed as markers for proliferating ocular progenitors (eyeless [ey]), early retinal progenitors (eyes absent [eya], sine oculis [so] and glass [gl]), and with additional lozenge [Lz] expression in late progenitors. Pax2, tramtrack (ttk), cut, glial cells missing (gcm) and reversed polarity (repo) are pro-glial in SCs. prospero (pros) marks the last PR (R7) and the SC progenitors. R7 fate is promoted by a pros/Ras positive feedback loop, whereas SC fate is promoted by a Pax2/Notch positive feedback loop. Anterior to the left.

Figure 3:. Cellular events during early pupal stages of Drosophila eye development.

Color code as in Figure 1 for retina (green) and Semper cells (blue). Light orange = primary pigment cells (PPCs), dark brown = interommatidial cells (IOCs). IOCs include the highly pigmented elongated secondary (2°) and hexagonal tertiary (3°) cells (= i, RPE). Interommatidial bristles indicated with circles.

Figure 4:. Final stages of Drosophila eye development.

(A) Same color code as Figure 3. (B) SC-based interretinular fiber locations in the adult eyes of Drosophila melanogaster (open rhabdomeres) and Meganyctiphanes norvegica (fused rhabdome). Rhabdomeres are indicated in dark green, while photoreceptor cell bodies are in light green.

Figure 5:. Junctions present in mature Semper cells.

(A) Top down and side view representations of different junctional complexes found in SCs. These include adherens junctions (zonula adherens, red), septate junctions (ladder-like junctions found beneath zonula adherens, blue), and gap junctions (yellow). Confocal images represent individual ommatidia stained for: the septate junction markers Neurexin IV (NrxIV, green) and Fasciclin 3 (Fas3, blue) and the adherens junction marker E-cadherin (E-cad, red) (top) or NrxIV (green) and hemi-desmosome marker β-integrin (β-int, magenta) (bottom).

Figure 6:. Hypothesized gene regulatory modules utilized by retinal support cells.

Phylogenetic tree depicts the relationships between taxa and species explored in the review with arthropods represented by five major lineages: insects, crustaceans, myriapods, the extinct trilobites, and chelicerates. The latter are represented by its only member with a compound eye, the horseshoe crab Limulus polyphemus. Schematics at branch tips depict generalized versions of the major eye types, ranging from compound eyes (arthropods) to independently evolved camera eyes of squids (cephalopods) and vertebrates (e.g. fish, birds, and mammals), as well as the independently derived eye types in the cnidarian species like Tripedalia cystophora (Cubozoa) and Cladonema radiatum (Hydrozoa). Bars to the right depict hypothesized ancient gene regulatory modules utilized in diverse visual organs as discussed in the text.