Proneural clusters of achaete-scute expression and the generation of sensory organs in the Drosophila imaginal wing disc.

Abstract

The proneural genes achaete (ac) and scute (sc) confer to Drosophila epidermal cells the ability to become sensory mother cells (SMCs). In imaginal discs, ac-sc are expressed in groups of cells, the proneural clusters, which are thought to delimit the areas where SMCs arise. We have visualized with the resolution of single cells the initial stages of sensory organ development by following the evolving pattern of proneural clusters and the emergence of SMCs. At reproducible positions within clusters, a small number of cells accumulate increased amounts of ac-sc protein. Subsequently, one of these cells, the SMC, accumulates the highest amount. Later, at least some SMCs become surrounded by cells with reduced ac-sc expression, a phenomenon probably related to lateral inhibition. Genetic mosaic analyses of cells with different doses of ac-sc genes, the sc expression in sc mutants, and the above findings show that the levels of ac-sc products are most important for SMC singling-out and SMC state maintenance. These products do not intervene in the differentiation of SMC descendants. The extramacrochaetae gene, an antagonist of proneural genes, negatively regulates sc expression, probably by interfering with activators of this gene.

Insights into neural stem cell biology from flies

“…These transcription factors drive ectodermal cells towards the neuroblast fate. The cell within the equivalence group that expresses the proneural genes to the highest level will adopt the neuroblast fate, while the other cells adopt an epidermal fate (Cubas et al 1991;Skeath & Carroll 1992;Skeath & Carroll 1994).…”

The Drosophila segmentation gene runt acts as a position-specific numerator element necessary for the uniform expression of the sex-determining gene Sex-lethal.

“…As sis-b, T4 interacts with the genes Sxl, da, and sis-a to initiate the female mode of development . As scute-alpha, T4 has been shown to interact with the genes h, emc, and da in the formation of the peripheral nervous system (bristles) (Botas 1982;Moscoso del Prado and Garcia-Bellido 1984a, b;DamblyChaudiere et al 1988;Garcia-Alonso and Garcia-Bellido 1988;Cubas et al 1991;Skeath and Carroll 1991).…”

“…A second possibility is the use of inhibitory gene products (Parkhurst et al 1990;Erickson and Cline 1991). The bHLH protein hairy (h) and the HLH protein extramacrochaetae (emc) inhibit the function of scute-alpha (T4) and achaete (T5) of the AS-C during bristle formation (Botas et al 1982;Moscoso del Prado and Garcia-Bellido 1984a, b;Garcia-Alonso and Garcia-Bellido 1988;Rushlow et al 1989;Ellis et al 1990;Garrell and Modolell 1990;Cubas et al 1991;Skeath and Carroll 1991). Consistent with a possible inhibitory role, emc and h are expressed at the time of Sxl initiation; the embryonic Sxl RNAs are detected from -2--4 hr of development and emc and h expression are also detected at this time (Ingham et al 1985;Salz et al 1989;Ellis et al 1990;Gartell and Modolell 1990).…”

Opposing inputs by Hedgehog and Brinker define a stripe ofhairyexpression in theDrosophilaleg imaginal disc

“…The bHLH transcription factors, Ac and Sc, are expressed in proneural clusters, groups of cells that roughly define the positions of future sensory structures in the adult (Cubas et al, 1991;Romani et al, 1989;Skeath and Carroll, 1991). Then, through local regulatory events controlled by the neurogenic genes, a cell(s) is selected from each proneural cluster to become a sensory organ precursor, which undergoes a few differential cell divisions (Calleja et al, 2002;Modolell, 1997).…”