Recruitment of cells into the Drosophila wing primordium by a feed-forward circuit of vestigial autoregulation.
The Drosophila wing primordium is defined by expression of the selector gene vestigial (vg) in a discrete subpopulation of cells within the wing imaginal disc. Following the early segregation of the disc into dorsal (D) and ventral (V) compartments, vg expression is governed by signals generated along the boundary between the two compartments. Short-range DSL (Delta/Serrate/LAG-2)-Notch signaling between D and V cells drives vg expression in ;border' cells that flank the boundary. It also induces these same cells to secrete the long-range morphogen Wingless (Wg), which drives vg expression in surrounding cells up to 25-30 cell diameters away. Here, we show that Wg signaling is not sufficient to activate vg expression away from the D-V boundary. Instead, Wg must act in combination with a short-range signal produced by cells that already express vg. We present evidence that this vg-dependent, vg-inducing signal feeds forward from one cell to the next to entrain surrounding cells to join the growing wing primordium in response to Wg. We propose that Wg promotes the expansion of the wing primordium following the D-V segregation by fueling this non-autonomous 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; D002465:Cell Movement / Q000502:physiology*; D004330:Drosophila / Q000196:embryology*; D029721:Drosophila Proteins / Q000235:genetics* / Q000378:metabolism* / Q000502:physiology; D004625:Embryo, Nonmammalian; D004742:Enhancer Elements, Genetic; D018507:Gene Expression Regulation, Developmental; D006706:Homeostasis; D008954:Models, Biological; D009687:Nuclear Proteins / Q000235:genetics* / Q000378:metabolism*; 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