The fly eye: Through the looking glass

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Abstract

<p id="P1">The developing eye-antennal disc of <i>Drosophila melanogaster</i> has been studied for more than a century and it has been used as a model system to study diverse processes such as tissue specification, organ growth, programmed cell death, compartment boundaries, pattern formation, cell fate specification, and planar cell polarity. The findings that have come out of these studies have informed our understanding of basic developmental processes as well as human disease. For example, the isolation of a white-eyed fly ultimately led to a greater appreciation of the role that sex chromosomes play in development, sex determination, and sex linked genetic disorders. Similarly, the discovery of the Sevenless receptor tyrosine kinase pathway not only revealed how the fate of the R7 photoreceptor is selected but it also helped our understanding of how disruptions in similar biochemical pathways result in tumorigenesis and cancer onset. In this article I will discuss some underappreciated areas of fly eye development that are fertile for investigation and are ripe for producing exciting new breakthroughs. The topics covered here include organ shape, growth control, inductive signaling, and right-left symmetry. </p>

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Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila.

G Halder, P Callaerts, W J Gehring (1995)

The Drosophila gene eyeless (ey) encodes a transcription factor with both a paired domain and a homeodomain. It is homologous to the mouse Small eye (Pax-6) gene and to the Aniridia gene in humans. These genes share extensive sequence identity, the position of three intron splice sites is conserved, and these genes are expressed similarly in the developing nervous system and in the eye during morphogenesis. Loss-of-function mutations in both the insect and in the mammalian genes have been shown to lead to a reduction or absence of eye structures, which suggests that ey functions in eye morphogenesis. By targeted expression of the ey complementary DNA in various imaginal disc primordia of Drosophila, ectopic eye structures were induced on the wings, the legs, and on the antennae. The ectopic eyes appeared morphologically normal and consisted of groups of fully differentiated ommatidia with a complete set of photoreceptor cells. These results support the proposition that ey is the master control gene for eye morphogenesis. Because homologous genes are present in vertebrates, ascidians, insects, cephalopods, and nemerteans, ey may function as a master control gene throughout the metazoa.

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Coordination of growth and cell division in the Drosophila wing.

Femmie de Vegt, Thomas P. Neufeld, Emma L. Johnston … (1998)

In most tissues, cell division is coordinated with increases in mass (i.e., growth). To understand this coordination, we altered rates of division in cell clones or compartments of the Drosophila wing and measured the effects on growth. Constitutive overproduction of the transcriptional regulator dE2F increased expression of the S- and M-phase initiators Cyclin E and String (Cdc25), thereby accelerating cell proliferation. Loss of dE2F or overproduction of its corepressor, RBF, retarded cell proliferation. These manipulations altered cell numbers over a 4- to 5-fold range but had little effect on clone or compartment sizes. Instead, changes in cell division rates were offset by changes in cell size. We infer that dE2F and RBF function specifically in cell cycle control, and that cell cycle acceleration is insufficient to stimulate growth. Variations in dE2F activity could be used to coordinate cell division with growth.

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Direct and long-range action of a wingless morphogen gradient.

G Struhl, M Zecca, K Basler (1996)

Wingless (Wg), a founding member of the Wingless/Int-1 (Wnt) family of secreted proteins, acts as a short-range inducer and as a long-range organizer during Drosophila development. Here, we determine the consequences of ectopically expressing (i) a wild-type form of Wg, (ii) a membrane-tethered form of Wg, and (iii) a constitutively active form of the cytosolic protein Armadillo (Arm), which normally acts to transduce Wg, and we compare them with the effects of removing endogenous Wg or Arm activity. Our results indicate that wild-type Wg acts at long range, up-regulating the transcription of particular target genes as a function of concentration and distance from secreting cells. In contrast, tethered Wg and Arm have only short-range or autonomous effects, respectively, on the transcription of these genes. We interpret these findings as evidence that Wg can act directly and at long range as a gradient morphogen during normal development.