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

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.

[1]  Ricardo Villares,et al.  Molecular genetics of the achaete-scute gene complex of D. melanogaster , 1985, Cell.

[2]  R. Villares,et al.  The achaete-scute gene complex of D. melanogaster: Conserved Domains in a subset of genes required for neurogenesis and their homology to myc , 1987, Cell.

[3]  A. Ghysen,et al.  The emergence of sense organs in the wing disc of Drosophila. , 1991, Development.

[4]  G M Rubin,et al.  Isolation and expression of scabrous, a gene regulating neurogenesis in Drosophila. , 1990, Genes & development.

[5]  P. Bryant Pattern formation in the imaginal wing disc of Drosophila melanogaster: fate map, regeneration and duplication. , 1975, The Journal of experimental zoology.

[6]  R. Pepperkok,et al.  Cell proliferation inhibited by MyoD1 independently of myogenic differentiation , 1990, Nature.

[7]  P. Simpson Notch and the choice of cell fate in Drosophila neuroepithelium. , 1990, Trends in genetics : TIG.

[8]  P. Simpson,et al.  Lateral inhibition and the development of the sensory bristles of the adult peripheral nervous system of Drosophila. , 1990, Development.

[9]  A. Ghysen,et al.  Genesis of the Drosophila peripheral nervous system. , 1989, Trends in genetics : TIG.

[10]  J. Modolell,et al.  Competence to develop sensory organs is temporally and spatially regulated in Drosophila epidermal primordia. , 1990, The EMBO journal.

[11]  V. Hartenstein,et al.  A dual function of the Notch gene in Drosophila sensillum development. , 1990, Developmental biology.

[12]  A. Garcı́a-Bellido,et al.  Cell-autonomous role of Notch, an epidermal growth factor homologue, in sensory organ differentiation in Drosophila. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[13]  P. Lawrence Development and determination of hairs and bristles in the milkweed bug, Oncopeltus fasciatus (Lygaeidae, Hemiptera). , 1966, Journal of cell science.

[14]  V. Wigglesworth,et al.  Local and General Factors in the Development of "Pattern" in Rhodnius Prolixus (Hemiptera) , 1940 .

[15]  S. Artavanis-Tsakonas The molecular biology of the Notch locus and the fine tuning of differentiation in Drosophila. , 1988, Trends in genetics : TIG.

[16]  J. Campos-Ortega Cellular interactions during early neurogenesis of Drosophila melanogaster , 1988, Trends in Neurosciences.

[17]  A. Garcı́a-Bellido,et al.  Parameters of the wing imaginal disc development of Drosophila melanogaster. , 1971, Developmental biology.

[18]  P. Simpson,et al.  The choice of cell fate in the epidermis of Drosophila , 1991, Cell.

[19]  D. Lindsley,et al.  Genetic variations of Drosophila melanogaster , 1967 .

[20]  J. Posakony,et al.  extramacrochaetae, a negative regulator of sensory organ development in Drosophila, defines a new class of helix-loop-helix proteins , 1990, Cell.

[21]  C. Bate Development of Sensory Systems in Arthropods , 1978 .

[22]  J. Modolell,et al.  The Drosophila extramacrochaetae locus, an antagonist of proneural genes that, like these genes, encodes a helix-loop-helix protein , 1990, Cell.

[23]  J. Campos-Ortega,et al.  Two groups of interrelated genes regulate early neurogenesis in Drosophila melanogaster , 2004, Roux's archives of developmental biology.

[24]  A. Garcı́a-Bellido,et al.  Genetic Analysis of the Achaete-Scute System of DROSOPHILA MELANOGASTER. , 1979, Genetics.

[25]  J. Modolell,et al.  Cross-regulatory interactions between the proneural achaete and scute genes of Drosophila. , 1991, Science.

[26]  J. Modolell,et al.  A unitary basis for different Hairy‐wing mutations of Drosophila melanogaster. , 1988, The EMBO journal.

[27]  A. Garcı́a-Bellido,et al.  Gene‐dose titration analysis in the search of trans‐regulatory genes in Drosophila. , 1982, The EMBO journal.

[28]  Y. Jan,et al.  daughterless, a Drosophila gene essential for both neurogenesis and sex determination, has sequence similarities to myc and the achaete-scute complex , 1988, Cell.

[29]  J. Modolell,et al.  Excess function Hairy-wing mutations caused by gypsy and copia insertions within structural genes of the achaete-scute locus of Drosophila , 1986, Cell.

[30]  J. Campos-Ortega,et al.  The expression of neurogenic loci in imaginal epidermal cells of Drosophila melanogaster. , 1984, Journal of neurogenetics.

[31]  D. Tautz,et al.  A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback , 1989, Chromosoma.

[32]  C. Rushlow,et al.  The Drosophila hairy protein acts in both segmentation and bristle patterning and shows homology to N‐myc. , 1989, The EMBO journal.

[33]  A. Garcı́a-Bellido,et al.  Developmental Analysis of the Achaete-Scute System of DROSOPHILA MELANOGASTER. , 1978, Genetics.

[34]  M. Sanders Handbook of Sensory Physiology , 1975 .

[35]  David Baltimore,et al.  A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins , 1989, Cell.

[36]  E. Macagno,et al.  Expression of achaete and scute genes in Drosophila imaginal discs and their function in sensory organ development. , 1989, Genes & development.

[37]  J. Modolell,et al.  Deletion analysis of the achaete-scute locus of Drosophila melanogaster. , 1987, Genes & development.

[38]  A. Ghysen,et al.  Two different sets of cis elements regulate scute to establish two different sensory patterns , 1989, Roux's archives of developmental biology.

[39]  Y. Jan,et al.  Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence , 1989, Cell.