The spatial organization of epidermal structures: hairy establishes the geometrical pattern of Drosophila leg bristles by delimiting the domains of achaete expression.
The spatial organization of Drosophila melanogaster epidermal structures in embryos and adults constitutes a classic model system for understanding how the two dimensional arrangement of particular cell types is generated. For example, the legs of the Drosophila melanogaster adult are covered with bristles, which in most segments are arranged in longitudinal rows. Here we elucidate the key roles of two regulatory genes, hairy and achaete, in setting up this periodic bristle pattern. We show that achaete is expressed during pupal leg development in a dynamic pattern which changes, by approximately 6 hours after puparium formation, into narrow longitudinal stripes of 3-4 cells in width, each of which represents a field of cells (proneural field) from which bristle precursor cells are selected. This pattern of gene expression foreshadows the adult bristle pattern and is established in part through the function of the hairy gene, which also functions in patterning other adult sense organs. In pupal legs, hairy is expressed in four longitudinal stripes, located between every other pair of achaete stripes. We show that in the absence of hairy function achaete expression expands into the interstripe regions that normally express hairy, fusing the two achaete stripes and resulting in extra-wide stripes of achaete expression. This misexpression of achaete, in turn, alters the fields of potential bristle precursor cells which leads to the misalignment of bristle rows in the adult. This function of hairy in patterning achaete expression is distinct from that in the wing in which hairy suppresses late expression of achaete but has no effect on the initial patterning of achaete expression. Thus, the leg bristle pattern is apparently regulated at two levels: a global regulation of the hairy and achaete expression patterns which partitions the leg epidermis into striped zones (this study) and a local regulation (inferred from other studies on the selection of neural precursor cells) that involves refinement steps which may control the alignment and spacing of bristle cells within these zones.
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Howard Hughes Medical Institute, Laboratory of Molecular Biology, University of Wisconsin-Madison 53706.
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Carroll
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D000818:Animals; D004331:Drosophila melanogaster / Q000196:embryology* / Q000235:genetics; D004817:Epidermis / Q000196:embryology*; D005121:Extremities; D005786:Gene Expression Regulation / Q000235:genetics*; D017344:Genes, Insect / Q000235:genetics*; D007150:Immunohistochemistry; D008855:Microscopy, Electron, Scanning; D008856:Microscopy, Fluorescence; D009024:Morphogenesis / Q000235:genetics