Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing.

Abstract

Adult Drosophila possess a large number of sensory organs, including large and small bristles and other types of sensilla, each arising from a single mother cell at particular positions in a reproducible pattern. Genetic studies have shown that sensory organ pattern formation is partly coordinated by a number of structurally similar, potential heterodimer-forming, helix-loop-helix (HLH) regulatory proteins. Here, by localizing regulatory gene expression during the development of normal and mutant imaginal discs, we show that two positive regulators of sensory neurogenesis, the proneural achaete and scute proteins, initially trans-activate each other and are transiently expressed in identical patterns, including clusters of wing ectodermal cells and the individual sensory mother cells that arise from them. Two negative regulators, hairy and extramacrochaete, suppress sensory neurogenesis by selectively repressing achaete and scute gene expression, respectively, but in different spatial domains and at different developmental stages. Surprisingly, we also find that the level of achaete-scute activity influences the level of ha/ry expression, thereby providing feedback control upon achaete-scute activity and sensory organ formation. Some or all of these interactions may involve specific dimerization reactions between different combinations of HLH proteins.

Dual role for Drosophila lethal of scute in CNS midline precursor formation and dopaminergic neuron and motoneuron cell fate

“…Although they partially overlap in expression, each gene has a unique pattern of midline expression. In the case of ac and sc, this contrasts with their expression in embryonic lateral neuroblasts and sensory organ precursors, where their expression closely overlaps, owing to use of a shared cis-regulatory region (Skeath and Carroll, 1991;Skeath et al, 1992). Regarding H-cell development, l(1)sc and sc, but not ac, are expressed in MP3 and could be involved in MP3 formation.…”

atonal is a proneural gene for a subset of olfactory sense organs in Drosophila

“…In the wing imaginal disc, ac and sc genes have very dynamic expression patterns. Initially, both genes express in groups of cells called proneural clusters and subsequently resolve into single-spaced sensory organ precursors (SOPs) which continue to express high levels of ac-sc until their division (Skeath & Carroll 1991). One SOP gives rise to one sensory structure.…”

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).…”