Development, Vol 107, Issue 2 389-405, Copyright © 1989 by Company of Biologists

JOURNAL ARTICLES

Development of adult sensilla on the wing and notum of Drosophila melanogaster

V Hartenstein and JW Posakony
Department of Biology, University of California San Diego, La Jolla 92093.

We have investigated the temporal pattern of appearance, cell lineage, and cytodifferentiation of selected sensory organs (sensilla) of adult Drosophila. This analysis was facilitated by the discovery that the monoclonal antibody 22C10 labels not only the neuron of the developing sensillum organ, but the accessory cells as well. The precursors of the macrochaetes and the recurved (chemosensory) bristles of the wing margin divide around and shortly after puparium formation, while those of the microchaetes and the stout and slender (mechanosensory) bristles of the wing margin divide between 9 h and 18 h after puparium formation (apf). The onset of sensillum differentiation follows the terminal precursor division within a few hours. Four of the cells in an individual microchaete organ are clonally related: A single first-order precursor cell divides to produce two second-order precursors; one of these divides into the neuron and thecogen cell, the other into the trichogen cell and tormogen cell. Along the anterior wing margin, two rounds of division generate the cells of the mechanosensory sensilla; here, no strict clonal relationship seems to exist between the cells of an individual sensillum. At the time of sensillum precursor division, many other, non-sensillum-producing cells within the notum and wing proliferate as well. This mitotic activity follows a spatially non-random pattern.
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				M Van Doren, P A Powell, D Pasternak, A Singson, and J W Posakony Spatial regulation of proneural gene activity: auto- and cross-activation of achaete is antagonized by extramacrochaetae. Genes & Dev., December 1, 1992; 6(12b): 2592 - 2605. [Abstract] [PDF]

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				S Campbell, M Inamdar, V Rodrigues, V Raghavan, M Palazzolo, and A Chovnick The scalloped gene encodes a novel, evolutionarily conserved transcription factor required for sensory organ differentiation in Drosophila. Genes & Dev., March 1, 1992; 6(3): 367 - 379. [Abstract] [PDF]

				P. Simpson, M. Bourouis, P. Heitzler, L. Ruel, M. Haenlin, and P. Ramain Delta, Notch, and shaggy: Elements of a Lateral Signaling Pathway in Drosophila Cold Spring Harb Symp Quant Biol, January 1, 1992; 57(0): 391 - 400. [Abstract] [PDF]

				J B Skeath and S B Carroll Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing. Genes & Dev., June 1, 1991; 5(6): 984 - 995. [Abstract] [PDF]

				P Cubas, J F de Celis, S Campuzano, and J Modolell Proneural clusters of achaete-scute expression and the generation of sensory organs in the Drosophila imaginal wing disc. Genes & Dev., June 1, 1991; 5(6): 996 - 1008. [Abstract] [PDF]