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First published online 28 May 2008
doi: 10.1242/dev.017053

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Timing of Wingless signalling distinguishes maxillary and antennal identities in Drosophila melanogaster

Centre de Biologie du Développement, UMR 5547 and IFR 109, Université de Toulouse and CNRS, 118 route de Narbonne, Bâtiment 4R3, 31062 Toulouse Cedex, France.

View larger version (61K): [in this window] [in a new window]   Fig. 1. Separate antennal and maxillary fields. (A-D) Exclusive expression domains of Dfd (red) and Cut (green) proteins in eye-antennal discs of (A) an early L2 larva; (B) a late L3 larva; (C) a prepupa; and (D) a pupal head after fusion of two eye-antennal and two labial (lb) discs (maxillary fields marked by arrows in D). (E,F) Clonal restriction established between antennal and maxillary territories in L2 is reflected by clones restricted either to the maxillary field (E;18/33) or to the posterior antennal field (F;12/33). Mitotic clones identified by the absence of GFP (broken lines) were situated relative to the maxillary territory identified by anti-Dfd (red). (G) Schematic representation of the eye-antennal disc, with its eye (grey), antennal (green) and maxillary (red) fields expressing Eyeless, Cut and Deformed proteins, respectively. Antennal discs are oriented with posterior towards the right and dorsal towards the bottom; e, a and mx indicate eye, antenna and maxillary primordia, respectively.

View larger version (117K): [in this window] [in a new window]   Fig. 2. Axial patterning of the antennal disc during larval and pupal development. Representative images with several marker combinations are presented for early-mid L2 (A,F,K,P), late L2 (B,G,L,Q), early L3 (C,H,M,R), late L3 larvae (D,I,N,S) and early pupae (E,J,O,T). (A-E) Inv (green) and Dfd (red) expression. (F-J) Inv/En (green) and ptc-lacZ (ptcZ, red) expression. Arrowheads mark maxillary Inv-expressing cells in C-E,H-J. (K-O) Wg (green) and dpp-lacZ (dppZ, red) expression. (P-T) Dll (green) and Hth (red) expression. Dll is co-expressed with Hth in both antennal (S) and maxillary primordia (T, inset). The results are summarised at the bottom in which Hth is indicated with a purple background. eL2, early L2; lL2, late L2; eL3, early L3; lL3, late L3. Antennal discs are oriented with posterior towards the right and dorsal towards the bottom; e, a and mx indicate eye, antenna and maxillary primordia, respectively.

View larger version (40K): [in this window] [in a new window]   Fig. 3. Temporally regulated wg expression distinguishes maxillary and antennal differentiation programs. (Top left) A schematic representation shows the normal temporal programs for dpp (red) and wg (green) expression in antennal and maxillary territories. (A,B) larval imaginal discs and adult heads harbouring mx-to-antennal transformations (mx>a). (Bottom left) The timing of wg mis-expression (see Materials and methods) is indicated by the striped green lines under the time bar. Each corresponds to a line in the results table, bottom right, indicating the effects of temporally regulated Wg mis-expression scored on Dan expression and on the adult mx>a transformation. Antennal discs are oriented with posterior towards the right and dorsal towards the bottom; a and mx indicate antenna and maxillary primordia, respectively.

View larger version (79K): [in this window] [in a new window]   Fig. 4. wg and ss are functionally linked in maxillary/antennal programs. (A) In wild-type L3/pupal transition, Wg (green) and Ss (red), but not Dll (blue), proteins are detected in maxillary (mx) cells. (B) In wild type, Dll is first detected in the mx primordium of white pre-pupae. (C,D) Both wg and ss induce a maxillary-to-antennal transformation through a mechanism involving reciprocal activation. (C) In wggof L3 larvae (ptc-GAL4>UAS-wgts shifted to 18°C at 5 days AEL), Ss (red) is precociously induced on the band of Wg-expressing cells (green) within the neo-antennal territory (mx>a). (D) In ssgof (ptc-GAL4>UAS-ss) L3 larvae, the mx>a transformation is associated with precocious Wg expression (green) overlying the band of Ss-expressing cells (red) in the mx field. (E,F) In ss- mutant pupae, normal expression is observed for Wg (green) or Dll (red) proteins. (G) Clone of pygo- cells (no green GFP marker, outlined) where nuclear Ss protein (red) is cell-autonomously absent from mutant maxillary cells. (H) Clone of Dll- cells [no green GFP marker (outlined) and no Dll (blue)] where nuclear Ss protein (red) is present in mutant maxillary cells. (E-H) These genotypes lead to reduction or loss of adult Mx palps (mx-). Antennal discs are oriented with posterior towards the right and dorsal towards the bottom; a and mx indicate antenna and maxillary primordia, respectively.

View larger version (71K): [in this window] [in a new window]   Fig. 5. Wg acts upstream of Ss and independently of it in transforming maxillary identity to antennal. (A1-A4) Light-microscope images of adult maxillary palps. (A1) Wild-type maxillary palps with their bordering row of bristles. (A2) ss- null homozygote shows strongly reduced maxillary palps. (A3) wggof; ss- double mutants (shifted to 18°C at 5 days AEL) generally have an enlarged structure, unlike either wggof neo-antennae or ss- stubs. These structures are positioned higher on the head, like neo-antennae (as seen in Fig. 3B). (A4) Same genotype as in A3, but with the maxillary palp replaced by distal leg with its distinctive claws. (B-E) Dan (green) and Dfd (red) expression in L3 E-A of (B) a wild-type antennal disc, (C) a wggof-induced transformation (ptc-GAL4>UAS-wgts shifted to 18°C at 5 days AEL), (D) a ssgof-induced transformation (ptc-Gal4>UAS-ss), (E) a wggof; ss- disc (shifted to 18°C at 5 days AEL) where Dfd (red) is excluded from the maxillary territory (arrowhead). (F,F') In ssgof discs harbouring large pygo- clones (no GFP), Dan (red) is expressed in a narrow band of maxillary cells (F, arrowhead) and Dfd expression (red) is maintained (F', arrowhead). (G) Schematic summary of results. Antennal discs are oriented with posterior towards the right and dorsal towards the bottom; a and mx indicate antenna and maxillary primordia, respectively.

View larger version (42K): [in this window] [in a new window]   Fig. 6. Summary model comparing features of antennal (first line) and maxillary (second line) programs, and indicating their changes in the maxillary-to-antennal transformation (third line). Larval L2, early L3 (eL3), late L3 (lL3) and pupal stages are indicated at the top. Stages permissive to Dan expression in maxillary territory are in green; refractory are in yellow. The stippled background indicates Dfd expression associated with maxillary development.

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