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Limb type-specific regulation of bric a brac contributes to morphological diversity

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

View larger version (41K): [in a new window]   Fig. 1. bab is required for joint formation in the distal leg and antenna. Wild-type cuticles of Drosophila leg (A), and antenna (B). Tarsal joints in the leg are indicated by arrows. The a4/a5 joint in the antenna is indicated by an arrowhead, the a5/arista joint by an arrow. (C) Tarsal joints (arrows) are fused or absent in the bab null leg (Godt et al., 1993). (D) The a4/a5 and a5/arista joints are absent in the bab null antenna (Godt et al., 1993). (E,F) The expression patterns of bab-lacZ during pupal stages are consistent with the phenotypes of the adult tarsal and antennal joints.

View larger version (65K): [in a new window]   Fig. 2. bab expression is dynamic during antenna and leg development. Bab (purple in all panels) is expressed throughout most of the Dll (green in all panels) expression domain in the early third instar in antenna (A,A') and leg (D,D'). By mid third instar, bab expression is lost in the distal-most part of the antenna (arrow in B') and two bab rings emerge (B,B'). At the same stage, bab expression is lost in the distal-most leg and a distal ring appears in the leg (E,E'). By late third instar, bab expression consists of two strong rings in the antenna (arrows in C and C') and four concentric rings in the tarsal region of the leg (arrows in F'). bab is also expressed in the presumptive coxa (cx) where it does not overlap with Dll.

View larger version (121K): [in a new window]   Fig. 3. bab expression depends on Dll in the antenna, leg and wing. Bab (purple in all panels) is not detected distally in Dll1/Dll3 hypomorphic antennal discs (A). Note that some Dll (green) is still present in the hypomorphic discs. Bab is not detected in (arrow) or around (arrowheads) a Dll null clone in the antenna (B). Double labeling of similar antennal clones for Dll and a myc marker indicates that Dll is lost cell-autonomously, i.e. loss of Dll expression corresponds with loss of Myc expression. The non cell-autonomous loss of Bab surrounding these Dll null antennal clones is correlated with activation of Dac (Dong et al., 2001), which we demonstrate here is a bab repressor. Bab also is not detected within (arrows) or around Dll null clones in the leg (C,C'). These clones were identified by absence of expression of the myc marker. The arrowhead indicates a portion of a Dll+ myc+/Dll+ myc+ "twin spot" in which Bab expression has been lost non cell-autonomously. The twinspots carry twice as many copies of the myc gene than the surrounding Dll+ myc+/Dll– heterozygous tissue and therefore stain more brightly. Although Bab expression is lost non cell-autonomously around Dll null clones in both antenna and leg discs, the mechanism by which this occurs in each may differ since Dll expression is also lost non cell-autonomously around the Dll null clones in the leg (J. C. and G. P., unpublished). Bab is lost cell-autonomously from a Dll null clone in the wing (arrow in D and D').

View larger version (85K): [in a new window]   Fig. 4. bab expression partially depends on Ss in the antenna and leg. (A,A') Proximal tarsal rings of Bab (purple in all panels) expression are lost in the ss null leg, while a distal ring of bab expression remains. (B,B') Expression of bab in the coxa is unaffected in ss mutants. Bab expression is partially lost in the ss null antenna, only one ring remains. Since these antennae are transformed toward leg, this ring is likely to represent the distal leg ring of bab. bab expression is partially derepressed distally in both the ss mutant leg and antenna. Expression of Dll appears normal in these discs (green in A and B).

View larger version (86K): [in a new window]   Fig. 5. Dac restricts bab expression in the leg. (A,A') Wild-type expression of Bab (purple in all panels) and Dac (green) in the leg disc. (B,B') bab expression is activated in a dac null clone (asterisk). The clone is marked by the absence of Myc (green). The wild-type twin spot (ts) of the clone possesses two copies of the myc transgene and therefore appears brighter green. Note that bab is non cell-autonomously activated in part of the twin spot near the clone (arrowhead). A portion of the endogenous bab ring of the first tarsal segment is indicated (t1). (D,D') bab expression is repressed by ectopic Dac (arrows) produced in the dpp pattern. The dpp pattern is dynamic (Masucci et al., 1990; Weigmann and Cohen, 1999), and Bab is not detected in cells that were exposed to high levels of Dac earlier in development and that continue to express moderate levels of Dac, probably due to autoregulation (arrowheads). (E,E') Bab expression expands proximally and its modulation between rings is greatly diminished in dac mutant leg discs. Dac appears to be expressed normally in bab null antennal (C) and leg (F) discs.

View larger version (106K): [in a new window]   Fig. 6. Sal restricts bab expression in the wing and haltere. (A) Wild-type expression of Bab (purple) and Sal (green) in the wing disc. (B,B',B'',B''') sal null clones (marked by the absence of green Myc staining) in the center of the wing pouch (arrowheads) lose Dll (blue) expression and activate Bab (red). (C) Wild-type expression of Sal (green) and Bab (purple) in the haltere. (D) A sal null clone in the haltere disc (arrowhead) also activates Bab.

View larger version (177K): [in a new window]   Fig. 7. bab expression is repressed by Dac, Sal and Hth in the antenna. (A) Wild-type expression of Bab (purple in all panels) and Dac (green in A,B,D). (B) Bab is derepressed in dac null clones in a3 (arrowheads). (C) bab expression expands proximally (arrowheads) into a3 in dac-lacZ/dac4 discs. Green is ß-galactosidase produced by the dac-lacZ element and marks where Dac would have been expressed. Note the extensive overlap (white) in C not seen in A. (D) bab is repressed by ectopic Dac produced in flipout clones (arrowheads). (E) Wild-type expression patterns of Bab and Sal (green). Sal-expressing cells were visualized by use of an anti-ß-galactosidase antibody in a sal-lacZ background. (F) bab is derepressed in sal null clones in a2 (arrowheads). Clones are marked by the absence of Myc (green). (G) bab is repressed by ectopic Sal (green) produced in a flipout clone (arrowheads). (H) Wild-type expression of Bab and Hth (green in H-J). (I) bab is activated in hth null clones (arrowheads). (J) bab is repressed by ectopic Hth (arrowheads) produced in the dpp pattern. The dpp pattern is dynamic (Masucci et al., 1990; Weigmann and Cohen, 1999), and Bab is not detected in cells exposed to high levels of Hth earlier in development (arrows in J).

View larger version (85K): [in a new window]   Fig. 8. Variations in bab derepression in Hth null antennae are correlated with variations in the resulting numbers of tarsal joints. Large hth null clones in the antenna were generated using a Minute (M) mutation on the hth+ chromosome. The hth+ M–/hth+ M– twinspots die, while the hth+ M–/hth– M+ heterozygous tissue surrounding the hth null clones grows poorly. Thus much of the antennal disc comprises hth– M+ tissue and is transformed toward leg. Under these conditions, Bab (purple) is often derepressed uniformly (A), and sometimes derepressed in a modulated pattern (C) resembling that found in the leg. (B) A partially transformed antenna with two joints (arrowheads). (D) A more completely transformed antenna with five tarsal segments and four tarsal joints (arrowheads). The relative frequencies at which these cuticular phenotypes arise suggest that the cuticle in B may derive from a disc with Bab expression similar to that found in A, while the cuticle in D may derive from a disc with Bab expression similar to that found in C. See text for details.

View larger version (1K): [in a new window]   Fig. 9. Both conserved and unique interactions regulate bab along the PD axis of the antenna and leg. bab is activated by Dll in both antenna and leg primordia. bab expression is ss dependent in the first through third tarsal segments (t1-3), but not in the fourth tarsal segment (t4) of the leg. The requirement of ss for bab expression in the antenna could not be assessed, because ss null antennae are transformed toward leg. The proximal boundary of bab expression is set by dac in both antenna and leg, but hth and sal also are required for bab repression in the antenna. dac also modulates bab expression levels between rings in both antenna and leg. The dependence of ss expression on Dll has been documented previously (Duncan et al., 1998), as have the dependence of sal (Dong et al., 2000) and dac (Dong et al., 2001) expression on Dll and hth and the mutual antagonism between Dll and dac in the leg (Dong et al., 2001). Solid lines indicate cell-autonomous effects that could be direct. The dotted line indicates that there is a non cell-autonomous component to inter-ring modulation of bab by dac in the antenna. See text for details.