The Cell Adhesion Molecules Roughest, Hibris, Kin of Irre and Sticks and Stones Are Required for Long Range Spacing of the Drosophila Wing Disc Sensory Sensilla (original) (raw)
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Genes & …, 1991
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.
Development, 2006
The basic helix-loop-helix (bHLH) proneural proteins Achaete and Scute cooperate with the class I bHLH protein Daughterless to specify the precursors of most sensory bristles in Drosophila. However, the mechanosensory bristles at the Drosophila wing margin have been reported to be unaffected by mutations that remove Achaete and Scute function. Indeed, the proneural gene(s) for these organs is not known. Here, we show that the zinc-finger transcription factor Senseless, together with Daughterless, plays the proneural role for the wing margin mechanosensory precursors, whereas Achaete and Scute are required for the survival of the mechanosensory neuron and support cells in these lineages. We provide evidence that Senseless and Daughterless physically interact and synergize in vivo and in transcription assays. Gain-of-function studies indicate that Senseless and Daughterless are sufficient to generate thoracic sensory organs (SOs) in the absence of achaete-scute gene complex function. ...
The emergence of sense organs in the wing disc of Drosophila
Development (Cambridge, England), 1991
We have examined the origin of a set of precisely located sense organs in the notum and wing of Drosophila, in transformant flies where lacZ is expressed in the progenitor cells of the sense organs (the sensory mother cells) and in their progeny. Here we describe the temporal pattern of appearance and divisions of the sensory mother cells that will form the eleven macrochaetes and the two trichoid sensilla of the notum, and five campaniform sensilla on the wing blade. The complete pattern of sensory mother cells develops in a strict sequence that extends over most of the third larval instar and the first 10 h after puparium formation. The delay between the onset of lacZ expression and the first differentiative division ranges from 30 h, in the case of the earliest mother cells, to 2 h for the latest mother cells. The first division shows a preferential orientation which is also specific for each sensory mother cell. Up to this stage, there is no marked difference between the three t...
Development, 1999
The nuclear proteins Spalt and Spalt-related belong to a conserved family of transcriptional regulators characterised by the presence of double zinc-finger domains. In the wing, they are regulated by the secreted protein Decapentaplegic and participate in the positioning of the wing veins. Here, we identify regulatory regions in the spalt/spalt-related gene complex that direct expression in the wing disc. The regulatory sequences are organised in independent modules, each of them responsible for expression in particular domains of the wing imaginal disc. In the thorax, spalt and spalt-related are expressed in a restricted domain that includes most proneural clusters of the developing sensory organs in the notum, and are regulated by the signalling molecules Wingless, Decapentaplegic and Hedgehog. We find that spalt/spalt-related participate in the development of sensory organs in the thorax, mainly in the positioning of specific proneural clusters. Later, the expression of at least ...
The EMBO Journal
The Drosophila adult cuticle displays a stereotyped pattern of sensory organs (SOs). Its deployment requires the expression of the achaete (ac) and scute (sc) genes. Their products confer to cells of epidermal primordia (imaginal discs and histoblasts) the ability to become SO precursors (SOPs). In imaginal discs, ac and sc expression is spatially restricted to cell clusters within which one or a few cells become SOP(s). With the help of ubiquitous sc expression provided at different developmental times by a heat shock-sc (HSSC) chimeric gene, we have analyzed the response of epidermal primordia to the proneural action of the sc product, and have tested whether the patterned distribution of ac/sc products is necessary to position SOs correctly within the epidermis. Each primordium responds to HSSC expression by developing SOs only during a characteristic developmental period. In the absence of the endogenous ac and sc genes, most SOs induced by HSSC are of the correct type and are l...
The Journal of Neuroscience, 1986
The ultrastructural differentiation and central projection of identified bristle mechanosensory neurons were examined in Drosophila mutants lacking action potentials. Two mutations, pm@ and mph, are known to block axonal conduction in centrally located neurons at high temperatures. Their effects on epithelial sensory cells, which are derived from imaginal disks during pupation, have not been determined. Furthermore, the pat+ nupfs double-mutant flies are lethal at all temperatures; thus the synergistic effect of these mutations on neurons has not yet been studied. It is possible to examine the above questions in genetic mosaics. By monitoring a reflex response involving identified bristle sensory cells, we found that the 2 mutations exert similar effects on these epithelial sensory cells as seen in central neurons. This also indicates that the action potential mechanisms in both epithelial sensory cells and central neurons are under similar genetic control. The parats nupP double-mutant sensory cells in mosaics are nonfunctional at all temperatures, providing an opportunity to examine, at the single cell level, the development of neurons with activity block. Ultrastructural specializations typical of epithelial sensory cells were found in the double-mutant cells. Cobalt backfilling experiments showed that central projections of these nonfunctional sensory cells were not altered, as compared with the active contralateral sensory cells. Therefore, blockage of the action potential mechanism in individual sensory cells has no effect on their pathfinding and arborization.
Cell, 2001
fers posterior (P) identity and Apterous confers dorsal (D) identity in the wing disc. P compartment cells lacking engrailed/invected activity do not respect the anteriorposterior boundary (García-Meyerhofstrasse 1 69117 Heidelberg Zecca et al., 1995). Likewise, dorsal cells lacking ap Germany activity fail to respect the dorsal-ventral (DV) boundary in the wing disc (Diaz-Benjumea and Cohen, 1993; Blair et al., 1994). One proposal to explain segregation of cells at compartment boundaries is that these selector Summary genes confer compartment-specific differences in cell affinity, perhaps by differential expression of cell adhe-Mechanisms to segregate cell populations play imporsion molecules (García-Bellido, 1972). tant roles in tissue patterning during animal develop-More recently, signaling between compartments has ment. Rhombomeres and compartments in the ectobeen implicated in producing the affinity differences that derm and imaginal discs of Drosophila are examples maintain the segregation of the distinctly specified cell in which initially homogenous populations of cells populations. Hedgehog signaling is asymmetric. P cells come to be separated by boundaries of lineage restricproduce Hedgehog, but are relatively insensitive to it, tion. Boundary formation depends in part on signaling whereas A cells are Hedgehog responsive (Basler and between the distinctly specified cell populations that Struhl, 1994; Tabata and Kornberg, 1994; Dominguez et comprise compartments and in part on formation of al., 1996; Ramirez-Weber et al., 2000)
Position-reading and the emergence of sense organ precursors in Drosophila
Progress in Neurobiology, 1994
Genetic analysis of development in Drosophila melanogaster has advanced our understanding of "position reading", where the expression of particular genes informs a cell of its position in the developing animal. The first step in localization of fly sense organs is the local expression of a gene conferring neural competence on epidermal cells. The four genes of the achaete-scute (AS-C) complex play crucial roles in the localization of sense organs. The resolution of local expression of AS-C genes along one dimension is about 10%; accuracy is improved by the balancing local expression of AS-C antagonist genes such as extramacrochaete. Position reading seems to depend primarily on such patterns of gene expression, and not upon the compartmental identity of the cells. No evidence has been found for differing roles of the four AS-C genes in the generation of sense organ progenitor cells or in the specification of neuronal properties of innervating neurons. The formation of each sense organ may be a unique case where the different proneural and neurogenic gene products have varying importance, and fortuitous local effects acting on this complex combination of factors have come to be important. The fly may be evolving from a flexible regular pattern to an inflexible irregular pattern strongly dependent on local factors, turning the fly into a crystallized system. (Written by R. Wayne Davies.) CONTENTS Abbreviations