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Proximodistal domain specification and interactions in developing Drosophila appendages

Department of Anatomy, University of Wisconsin, Madison, WI 53706, USA

View larger version (23K): [in a new window]   Fig. 1. Comparison of gene expression patterns along the PD axes of wild-type leg and antennal discs. (A) Schematics of adult Drosophila antenna (top) and leg (bottom). Arrows indicate homologous domains (Postlethwait and Schneiderman, 1971). The first antennal segment (a1) is homologous to the coxa (cx) of the leg. The second antennal segment (a2) is homologous to the trochanter (tr) of the leg. The third antennal segment (a3) is homologous to the femur (fe), tibia (ti) and first tarsal segment (t1). The arista (ar) and its base (a4 and a5) are homologous to the second through fifth tarsal segments (t2-5) and the tarsal claw (cl). (B,D) Immunohistochemical labeling to visualize Dac (red) and Dll (green) protein in mature third instar antennal (B) and leg (D) discs. The overlap is yellow. The dac expression domain partially overlaps that of Dll in the leg, but lies completely within the Dll domain in the antenna. (C,E) Dac (red) and Hth (blue) protein in mature third instar antennal (C) and leg (E) discs. The overlap is pink. Dac and Hth expression are largely exclusive in the leg, but the two genes are coexpressed in the antenna. (F) Summary of late third instar antenna (top) and leg (bottom) expression patterns. The trochanter expression of Dll is not initiated until fairly late in development, during the third larval instar. Broken lines demarcate homologous segments as determined by transformation phenotypes (Postlethwait and Schneiderman, 1971).

View larger version (111K): [in a new window]   Fig. 2. Mutual antagonism between dac and Dll in the leg. dac is derepressed in a Dll null clone (arrow in A,A'), while Dll is derepressed in a dac null clone (arrows in B,B'). Dac is in red. Dll protein is green. The overlap of Dll and Dac is yellow.

View larger version (82K): [in a new window]   Fig. 3. Tsh and not Hth, is a dac repressor in the leg. (A,A') Clonal loss of hth (green in A-C) does not lead to derepression of dac (red in all panels) in the proximal leg (arrows). Ectopic expression of Hth either in flipout clones induced late in development (B,B') or using a dpp-GAL4 driver that is active from early stages onwards (C,C') does not repress dac in the medial leg (arrows in both). In both cases, Hth was detected via a green fluorescent protein (GFP) tag. (D,D') In contrast, ectopic expression of Tsh in the medial leg represses dac (arrows). Clones of cells ectopically expressing Tsh were detected by simultaneously flipping on GFP (blue).

View larger version (72K): [in a new window]   Fig. 4. Dac does not antagonize either Dll or hth expression in the antenna. Both Dll (green in A,A') and Hth (green in B,B') expression are normal in dac-null clones (arrows) in the antenna. Dac is in red. (C,D) Increasing the duration, level and area of dac expression in the antenna using a dpp-GAL4 driver induces the formation of medial leg structures in the antenna. (D) A higher magnification image of the portion of the antenna boxed in C. Two bracted bristles characteristic of the medial and distal leg are indicated with arrows in D.(E) High-magnification image of the second and part of the third segments of a wild-type antenna. None of the antennal bristles normally possess bracts. (F) High-magnification image of the distal portion of the femur of a wild-type leg. Note the bracts (arrows) present at the base of each bristle.

View larger version (138K): [in a new window]   Fig. 5. Differential regulation of dac by Dll along the PD axis of the antenna. Dac (red in all panels) expression expands distally in a Dll1/Dll3 hypomorphic antennal disc (A,A'). Dll protein (green in all panels) still is detected in these mutants. The overlap of Dll and Dac is yellow in all panels. In the antenna, the consequences to dac expression of loss of Dll vary with the PD position of the clone (B,B',C and C'). dac expression is activated non-cell autonomously (arrowheads in B') around a Dll-null clone (arrow in B,B') in a4. By contrast, dac expression is lost in a Dll-null clone in a3 (arrowhead in C,C').

View larger version (109K): [in a new window]   Fig. 6. Hth regulation of dac in the antenna. (A,A',B,B') Dac expression (red in all panels) is activated in hth (green) null clones in the antenna. Dac expression is activated distally (arrow in A,A'), medially (arrowhead A,A') and proximally (arrows in B,B') in hth-null clones. (C,C') Ectopic Hth produced in flipout clones in a3 (the normal dac expression domain) either has no effect on dac expression (arrow in C,C') or weakly represses dac (arrowhead in C,C'). The overlap of Dac and Hth is yellow.

View larger version (18K): [in a new window]   Fig. 7. Proximal, medial and distal domains antagonize one another in the leg, but not in the antenna. Schematics of the leg and the antenna with Hth-expressing domains indicated in blue, Dac-expressing domains in red, and Dll-expressing domains in green. Mutually antagonistic interactions between proximal and medial and between medial and distal maintain domain identity in the leg. By contrast, the same genes do not antagonize the expression of one another in the antenna. This results in the overlapping expression of hth, Dll and dac, and the absence of a functional medial domain defined by dac. Our data are consistent with Dll and Hth repressing leg-specific expression of dac in the antenna and with both Dll and Hth being required for the normal antennal expression of dac in a3.