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Distal-less and homothorax regulate multiple targets to pattern the Drosophila antenna

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

View larger version (54K): [in a new window]   Fig. 1. Dll, hth and ss mutants all exhibit antenna to leg transformations. (A) Wild-type antenna. (B) Dll3/Dll7 hypomorphic antenna in which distal a3 and the arista are transformed toward leg. (C) A large hthP2 clone in the antenna results in transformation of a1 to arista into leg structures. (D) ss null antenna of genotype Df(3R)ssD114.4/ssD114.9. a1-a5, antennal segments 1-5: ar, arista.

View larger version (75K): [in a new window]   Fig. 2. ss is regulated by Dll and hth. (A) Wild type antenna disc showing Hth protein (green) and Dll protein (red). (B) ss null antenna disc of genotype Df(3R)ssD114.4/ssD114.9 in which Hth and Dll expression is normal. (C) Wild-type expression of ss in a late third instar leg disc. (D) Expression of ss is induced in the distal leg (arrow) by ectopic expression of Hth. (E) Wild-type expression of ss in a late third instar wing disc. (F) Expression of ss is induced in the wing pouch (arrows) by ectopic expression of Hth.

View larger version (76K): [in a new window]   Fig. 3. cut, ato, sal and dac are differentially expressed in antenna and leg discs. Wild-type expression of cut (A,E), ato (B,F), sal (C,G) and dac (D,H) in wild-type antenna (A-D) and leg (E-F) discs.

View larger version (55K): [in a new window]   Fig. 4. The a5-arista joint is defective in dac null antennae. (A) Wild-type, and (B) dac3/dac4 antenna. Arrowheads indicate the location of the a5-arista joint.

View larger version (101K): [in a new window]   Fig. 5. ato is regulated by Dll and hth, but not ss and the a2-a3 joint is defective in ato null antenna. (A) Wild type, (B) ato1 and (C) Df(3R)ssD114.4/ssD115.7 second antennal segments (a2). Arrows in A and C indicate the circular outline of the a2-a3 joint which is normal in ss mutant antenna, but absent in the ato1 antenna in B. ato expression is lost in a hypomorphic Dll antenna (D) and in hth null clones (F and F'), but not in a ss null (Df(3R)ssD114.4/ssD114.9) antenna disc (E). Ato is green in all panels. Hth is red in F. Arrowheads in D and E indicate Ato in the eye.

View larger version (64K): [in a new window]   Fig. 6. sal mutants exhibit defects in the a2 cuticle and in the a2-a3 joint necessary for audition. (A) salFCK–25/Df(2L)32FP-5 FRT40A antenna. a2 is reduced in size distally (arrowheads), exposing the stalk (arrow) of a3 that inserts into a2. (B) Optical section of the interior of a wild-type a2. The circular outline of the a2/a3 joint to which the chordotonal organs of the JO attach is indicated (arrowhead). (C) Optical section of the interior of an a2 in which a sal/salr null clone has been induced, and the circular outline of the a2/a3 joint is disrupted (arrowhead). (D) Wild-type expression of Sal (red) and Ato (green) in the eye-antennal disc. (E) Expression of Sal (red) and Ato (green) in a salFCK–25/Df(2L)32FP-5 FRT40A antenna disc. Sal is lacking in the antenna disc, but Ato is still expressed. Note that Sal is expressed normally in the eye disc of this allelic combination. (F) Expression of Sal (red) in an ato1 eye-antennal disc. Sal is lost from the eye disc, but expressed normally in the antenna. (G) Sal (red) and Dac (blue) expression in a ss null (Df(3R)ssD114.4/ssD114.9) eye-antennal disc. Both are expressed normally.

View larger version (63K): [in a new window]   Fig. 7. cut expression in the antenna is dependent on hth, but not on Dll or ss. (A,A'). Expression of Cut (red) and Hth (green) in a wild-type antenna disc. (B,B'). Cut (red) expression is reduced (arrowheads) or lost (arrows) in hth null clones in the antenna disc. (C,C',C'') Cut (red) is expressed in a Dll null clone in the antenna. Dll is in blue. (D) The allelic combination of DllGAL4/Dll3 results in loss of the arista and transformation of a3 toward leg. a2 is present and has a normal cuticle. (E) Cut (red) is derepressed in the center of a Dll hypomorphic antenna disc. (F) Cut (red) is expressed normally in a ss null (Df(3R)ssD114.4/ssD114.9) antenna disc.

View larger version (14K): [in a new window]   Fig. 8. The genetic hierarchy that governs antenna development. (A) Dll and hth, probably in conjunction with exd, are required for the antennal expression of ss, dac, ato and sal, which in turn are required for various aspects of antennal differentiation. Dll is required independently for the activation of arista-less (al), Bar and bab (Campbell and Tomlinson, 1998; Chu et al., 2002; Gorfinkiel et al., 1997; Kojima et al., 2000), while hth is required independently for the activation of cut. (B) In addition to activating genes required for specific aspects of antennal differentiation, the homeotic functions of Dll, hth, exd and ss also include repression of distinct aspects of leg differentiation. For instance, while Dll and hth are required for activation of the low level expression of dac in a3, they also prevent the high level dac expression necessary for medial leg differentiation (Dong et al., 2001). hth can also repress dac independent of Dll since ectopic dac expression is observed in hth null clones in a1 and the surrounding head capsule (Dong et al., 2001). Since hth is required for proximal leg as well as antenna differentiation, hth null clones in the proximal antenna are transformed to medial rather than proximal leg structures (P. D. S. D., J. C. and G. P., unpublished observations). ss is downstream of Dll and hth and is required for the repression of distal leg fates (Duncan et al., 1998) (Ian Duncan, personal communication) (this work). (C) Summary of the antennal expression patterns and relationships among Dll, hth, ss, sal, ato, dac and cut.