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. 2022 May 5;221(1):iyac041.
doi: 10.1093/genetics/iyac041.

The early history of the eye-antennal disc of Drosophila melanogaster

Brandon P Weasner  1 , Justin P Kumar  1
Affiliations

The early history of the eye-antennal disc of Drosophila melanogaster

Brandon P Weasner et al. Genetics. .

Abstract

A pair of eye-antennal imaginal discs give rise to nearly all external structures of the adult Drosophila head including the compound eyes, ocelli, antennae, maxillary palps, head epidermis, and bristles. In the earliest days of Drosophila research, investigators would examine thousands of adult flies in search of viable mutants whose appearance deviated from the norm. The compound eyes are dispensable for viability and perturbations to their structure are easy to detect. As such, the adult compound eye and the developing eye-antennal disc emerged as focal points for studies of genetics and developmental biology. Since few tools were available at the time, early researchers put an enormous amount of thought into models that would explain their experimental observations-many of these hypotheses remain to be tested. However, these "ancient" studies have been lost to time and are no longer read or incorporated into today's literature despite the abundance of field-defining discoveries that are contained therein. In this FlyBook chapter, I will bring these forgotten classics together and draw connections between them and modern studies of tissue specification and patterning. In doing so, I hope to bring a larger appreciation of the contributions that the eye-antennal disc has made to our understanding of development as well as draw the readers' attention to the earliest studies of this important imaginal disc. Armed with the today's toolkit of sophisticated genetic and molecular methods and using the old papers as a guide, we can use the eye-antennal disc to unravel the mysteries of development.

Keywords: Drosophila; FlyBook; eye-antennal disc.

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Figures

Fig. 1.
Fig. 1.
Fate map of the eye-antennal disc and adult head. Two eye-antennal discs fuse together during pupal development and comprise most of the external structures of the adult head. a) The eye-antennal disc is divided into several individual neighborhoods. These domains give rise to the compound eye (eye), the ocelli (oc), the antenna (ant), the maxillary palps (mp), and all surrounding head epidermis (he). b) The structures that develop within the eye-antennal disc are mapped onto the right side of the adult head. c) A view of the right eye of the compound eye. It contains approximately 750 ommatidia that are organized into 32–34 vertical columns.
Fig. 2.
Fig. 2.
Structure of the eye-antennal imaginal discs. a–c) The eye-antennal disc is comprised of 3 distinct cell layers. The DP is a pseudo-stratified epithelium consisting of columnar shaped cells. It is covered by a similar sized sheet of squamous cells called the PE. These cells layers are joined together along their edges by a thin layer of cuboidal cells called the margin (M).
Fig. 3.
Fig. 3.
Imaginal disc transplantation system. George Beadle and Boris Ephrussi developed a disc transplantation system that was later used by Ernst Hadorn to address theories of tissue determination. In this example, an eye-antennal imaginal disc is dissected and removed from a donor larva. It is then transplanted into a third instar larval host. As the host undergoes metamorphosis into an adult, the donor eye-antennal disc will be transformed into half of an adult head, which can be recovered from the abdomen of the adult fly. This schematic is idealized. Please see the papers cited within this review for the original photographs.
Fig. 4.
Fig. 4.
Imaginal disc fate in Drosophila is determined during embryogenesis. Embryos of different genotypes are first bisected. The anterior of one type of embryo was mixed with the posterior half of a different embryo type. The cells are then dissociated and then mixed to form an aggregate which are then transplanted into host adults. As the adults age, the transplanted cells would give rise to imaginal discs. A recovered eye-antennal disc was comprised of cells from the anterior half of the embryo. A, anterior; P, posterior. This schematic is idealized. Please see the papers cited within this review for the original photographs.
Fig. 5.
Fig. 5.
Determination of Drosophila imaginal discs. Ernst Hadorn used the larval disc transplantation system developed by George Beadle and Boris Ephrussi to test theories of tissue determination. In this example, an eye-antennal disc is removed from a donor larva, fragmented, and transplanted into a larval host. Upon metamorphosis the fragment will regenerate the lost parts of the disc will give rise to half of the adult head. Since the identity of the eye-antennal disc and the adult head is synchronized, the identity of the tissue is said to have been determined at the time of transplantation. This schematic is idealized. Please see the papers cited within this review for the original photographs.
Fig. 6.
Fig. 6.
Fragments of the eye-antennal disc give rise to adult head structures. a–d) Light microscope images taken from Lebovitz and Ready (1986). a) A wild-type eye-antennal disc showing position of future cut. b) A fragment of the eye-antennal disc containing just the antenna and anterior part of the eye disc. This fragment lacks photoreceptor clusters and the morphogenetic furrow. It will be transplanted into donor adults and larva as shown in Fig. 7. c, d) Adult tissue recovered from the abdomens of adults after metamorphosis.
Fig. 7.
Fig. 7.
The retinal determination network of Drosophila. a) Scanning electron micrograph (SEM) of a wild-type compound eye. b, c) SEM images of loss-of-function eyeless mutants in which the eyes are either completely missing (b) or severely reduced in size (c). d) Forced expression of eyeless in nonretinal tissues results in the formation of ectopic eyes. e) The core members of the retinal determination network are depicted and include a set of DNA binding proteins and transcriptional activators. Depicted are 2 Pax6 transcription factors Twin of Eyeless (Toy) and Eyeless (Ey), the SIX protein homolog Sine Oculis, the Eyes Absent (Eya) transcriptional activator/phosphatase, and Dachshund (Dac) a member of the Ski/Sno family of transcriptional repressors.
Fig. 8.
Fig. 8.
Transdetermination of Drosophila imaginal discs fragments. In this paradigm, Ernst Hadorn fragmented imaginal discs and transplanted small pieces of the discs into host larvae. Under most circumstances, these fragments would regenerate and give rise to the appropriate adult structure (see Fig. 6 for an original image from Lebovitz and Ready, 1986). However, in a small number of instances, the imaginal disc would produce adult structures that would normally be derived from different imaginal discs. In this example, the regenerating portion of an eye-antennal disc fragment would transdetermine into a wing. The resulting adult tissue is a mosaic of head and wing tissue. Loss of several gene mimic this transdetermination event. This schematic is idealized. Please see the papers cited within this review for the original photographs.
Fig. 9.
Fig. 9.
Map of transdetermination events. The ability of each imaginal disc to transdetermine into another disc is quantitatively and qualitatively unique when compared to all other imaginal discs. For example, the antennal portion can transdetermine into wing, leg, labial, and genital discs while the eye portion can only adopt the fate of the wing disc. Some transdetermination events are unidirectional (i.e. haltere-to-wing) while others are bidirectional (antenna-to-leg and leg-to-antenna). And some events occur at relatively high frequencies (i.e. leg-to-wing) while others are rare events (i.e. antenna-to-genital).
Fig. 10.
Fig. 10.
Growth characteristics for the imaginal discs of Drosophila. Each external appendage (and hence the imaginal disc from which it is derived) has a distinct final size. Several factors influence how the final size of each adult structure is achieved. These include starting with unique number of cells, initiating proliferation at different times during the first larval instar, and doubling in size at distinct rates. E, eye; A, antenna; W, wing; H, haltere; L, leg.
Fig. 11.
Fig. 11.
The morphogenetic furrow patterns the eye-antennal disc. a–f) Light microscope images of third larval instar eye-antennal discs. a) At the L2/L3 transition, there are no signs of photoreceptor development. b–e) As development proceeds, the morphogenetic furrow initiates patterning at the posterior margin of the disc. It traverses in the anterior direction until it reaches the border of the eye and antennal fields. As it moves across the eye field, the sea of undifferentiated cells is transformed into orderly rows of periodically spaced unit eyes. f) A higher magnification view of a late third larval instar eye-antennal disc showing the transformation of an undifferentiated field into an ordered array.
Fig. 12.
Fig. 12.
The assembly line of photoreceptor development. The first mitotic wave produces many cells. The morphogenetic furrow sweeps up a fraction of those cells and organizes them into a periodic array of 5-cell preclusters. The first cell of the precluster to have its fate specified is the R8. This is followed by the specification of the R2/5 and the R3/4 pairs. All cells that are not incorporated into the precluster undergo one final round of cell division called the second mitotic wave. Three cells from the second mitotic wave are added to the growing cluster and are specified as the R1/6 and R7 photoreceptors. At this point in development, the ommatidium has a symmetrical arrangement.
Fig. 13.
Fig. 13.
Organization of the ommatidium. During larval development, the symmetrical arrangement of the ommatidium is broken and the photoreceptors are organized into the shape of an asymmetric trapezoid. The trapezoids in the dorsal half of the retina are mirror images of those that lie within the ventral half. These mirror images are the products of different chirality and rotation events. The point at which the dorsal and ventral compartments meet in the eye is called the equator. RD, right eye, dorsal compartment; LD, left eye, dorsal compartment; RV, right eye, ventral compartment; LV, left eye, ventral compartment.
Fig. 14.
Fig. 14.
The eye mutants of Drosophila reveal the roles of genes in development. a–d) SEM of adult Drosophila heads. a, b). Mutations that affect tissue specification, growth, patterning, and/or R8 cell often result in compound eyes that are missing or severely reduced in size. c, d) The loss of genes that affect later stages of ommatidial assembly (i.e. R2/R5, R3/4, R1/6, and R7 photoreceptors, cone cells, and pigment cells) result in large compound eyes that are “roughened” or “glazed” in appearance. Mutations that eliminate the bristle cells result in compound eyes that have a “balding” appearance (not shown).
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