The homeo domain protein rough is expressed in a subset of cells in the developing Drosophila eye where it can specify photoreceptor cell subtype.

Abstract

The Drosophila homeo box gene rough is required in photoreceptor cells R2 and R5 for normal eye development. We show here that rough protein expression is limited to a subset of cells in the developing retina where it is transiently expressed for 30--60 hr. The rough protein is first expressed broadly in the morphogenetic furrow but is rapidly restricted to the R2, R3, R4, and RS precursor cells. Ubiquitous expression of rough under the control of the hspTO promoter in third-instar larvae supresses the initial steps of ommatidial assembly.Structures derived from other imaginal discs are not affected. Ectopic expression of rough in the R7 precursor, through the use of the sevenless promoter, causes this cell to develop into an R1-6 photoreceptor subtype; however, this cell still requires sevenless function for its neural differentiation. Taken together with previous analyses of the rough mutant phenotype, these results suggest that the normal role of rough is to establish the unique cell identity of photoreceptors R2 and R5.[Key Words: Homeo domain; eye development; Drosophila melanogaster; rough; ectopic expression; sevenless] Received January 9, 1990; revised version accepted February 21, 1990.The Drosophila eye is composed of -800 unit eyes called ommatidia. Each ommatidium contains a stereotyped arrangement of 20 cells in which each cell can be identified by its morphology and position (Dietrich 1909;Ready et al. 1976). Eight of these cells are photoreceptors: six outer cells, R1-R6, and two smaller central cells, R7 and R8. The adult retina develops from an undifferentiated epithelial monolayer, the eye imaginal disc, beginning in the third instar larva (Ready et al. 1976; Tomlinson and Ready 1987aj. Organization of cells into ommatidia begins in an indentation in the disc, called the morphogenetic furrow, which moves from posterior to anterior across the eye disc over a 2-day period. Thus, ommatidial assembly occurs asynchronously across the anterior-posterior axis of the eye disc such that each column of developing ommatidia is -2 hr more developmentally advanced than the adjacent column to the anterior. In the morphogenetic furrow, five cells form a circular precluster that eventually gives rise to five of the eight photoreceptor cells of an ommatidium. Neuronal differentiation of these five photoreceptor precursors occurs in a stereotyped order: R8, R2, and R5, and R3 and R4 (Tomlinson and Ready 1987a An eye disc from a larva homozygous for the null rough allele ro x63 stained with MAbro 1. ro ~63 is a small X-ray-induced deletion near the 5' end of the rough-coding region that results in a frameshift after the thirty-first codon {U. Heberlein, unpubl.). The lack of detectable rough protein in this disc demonstrates the specificity of MAbrol. The arrowhead in A marks the position of the morphogenetic furrow where rough protein was first detected, rough protein was localized in the cell nucleus. Magnifications in A, A inset, and B are 250 x, 350 x, and 200 x, respectively. Phase-contrast images of singl...

Signal integration during development: Insights from the Drosophila eye

“…These rough mutants also show non-cell autonomous defects in ommatidial assembly, presumably because R2 and R5 are important sources for secreted Spitz (Tomlinson et al, 1988). Not far behind the MF, strong Rough expression is maintained only in R2 and R5, and weak expression can be seen in R3 and R4 (Kimmel et al, 1990). Thus, Rough is the key to establishing R2 and R5 cell fates.…”

Regulation of multimers via truncated isoforms: a novel mechanism to control nitric-oxide signaling

“…Cobalt sulfite staining of retinal sections was performed as described by Wolff and Ready (1991). Scanning electron microscopy was performed at the State University of New York-Stony Brook Imaging Center, essentially as described by Kimmel et al (1990).…”

A genetic screen for modifiers of the lats tumor suppressor gene identifies C-terminal Src kinase as a regulator of cell proliferation in Drosophila

“…Fixation, antibody staining, and scanning electron microscopy were performed using standard methods (Tomlinson and Ready, 1987;Kimmel et al, 1990). BrdU incorporation was performed as described (Huang et al, 1999b).…”