Control of Drosophila wing growth by the vestigial quadrant enhancer.
Following segregation of the Drosophila wing imaginal disc into dorsal (D) and ventral (V) compartments, the wing primordium is specified by activity of the selector gene vestigial (vg). In the accompanying paper, we present evidence that vg expression is itself driven by three distinct inputs: (1) short-range DSL (Delta/Serrate/LAG-2)-Notch signaling across the D-V compartment boundary; (2) long-range Wg signaling from cells abutting the D-V compartment boundary; and (3) a short-range signal sent by vg-expressing cells that entrains neighboring cells to upregulate vg in response to Wg. Furthermore, we showed that these inputs define a feed-forward mechanism of vg autoregulation that initiates in D-V border cells and propagates from cell to cell by reiterative cycles of vg upregulation. Here, we provide evidence that this feed-forward mechanism is required for normal wing growth and is mediated by two distinct enhancers in the vg gene. The first is a newly defined ;priming' enhancer (PE), that provides cryptic, low levels of Vg in most or all cells of the wing disc. The second is the previously defined quadrant enhancer (QE), which we show is activated by the combined action of Wg and the short-range vg-dependent entraining signal, but only if the responding cells are already primed by low-level Vg activity. Thus, entrainment and priming constitute distinct signaling and responding events in the Wg-dependent feed-forward circuit of vg autoregulation mediated by the QE. We posit that Wg controls the expansion of the wing primordium following D-V segregation by fueling this autoregulatory mechanism.
Zecca
Myriam
M
Howard Hughes Medical Institute, Department of Genetics and Development, Columbia University College of Physicians and Surgeons, 701 W 168th Street, New York, NY 10032, USA.
Struhl
Gary
G
D000818:Animals; D030801:Animals, Genetically Modified; D019521:Body Patterning / Q000235:genetics; D004330:Drosophila / Q000196:embryology* / Q000235:genetics*; D029721:Drosophila Proteins / Q000235:genetics* / Q000502:physiology; D004625:Embryo, Nonmammalian; D004742:Enhancer Elements, Genetic / Q000502:physiology*; D018507:Gene Expression Regulation, Developmental; D006706:Homeostasis / Q000502:physiology; D008954:Models, Biological; D009687:Nuclear Proteins / Q000235:genetics*; D011518:Proto-Oncogene Proteins / Q000502:physiology; D014921:Wings, Animal / Q000196:embryology* / Q000378:metabolism; D051155:Wnt1 Protein
D029721:Drosophila Proteins; D009687:Nuclear Proteins; D011518:Proto-Oncogene Proteins; D051155:Wnt1 Protein; C095064:vg protein, Drosophila; C074622:wg protein, Drosophila