Drosophila antenna development

The adult fruit fly antenna consists of six segments. From proximal to distal, these are called a1, a2, a3, a4, a5 and arista (a6; Fig. 1A). The different segments of the antenna serve distinct sets of functions including hygrosensation (arista), thermosensation (a3), olfaction (a3), and audition (arista and a2) (Carlson, 1996; Eberl, 1999; Goepfert and Robert, 2001; Sayeed and Benzer, 1996). Although the various functions of the antenna have been studied in detail, there is relatively little known about the genetic hierarchy that governs antenna formation. We are investigating what genes are involved and how they are involved in patterning the Drosophila antenna to understand how particular peripheral sensory structures are generated along the proximodistal (PD) axis of the antenna. In the antenna, as in other appendages, the process of pattern formation requires both limb fate information and PD information. The homeodomain transcription factor-encoding genes, Distal-less (Dll) and homothorax (hth), provide both. Losing the function of either Dll or hth, results in deletions of the distal and proximal domains, respectively (Casares and Mann, 1998; Cohen and Jurgens, 1989; Pai et al., 1998). In addition, coexpression of Dll and hth is required for the specification of antenna fate (Dong et al., 2000). Losing the function of either gene results in antenna to leg transformation (Fig. 1B,C) (Casares and Mann, 1998; Cohen and Jurgens, 1989; Dong et al., 2000; Sato, 1984; Sunkel and Whittle, 1987). One might expect the targets of Dll or hth for PD patterning to be expressed in both the antenna and the leg. Consistent with this, the Dll targets, bric a brac (bab), aristaless (al), and BarH1/BarH2, are expressed and required in both the distal antenna and leg (Campbell and Tomlinson, 1998; Godt et al., 1993; Kojima et al., 2000; Schneitz et al., 1993). In contrast, the targets of Dll and hth involved in antenna specification would be predicted to have antenna-specific patterns of expression. Consistent with this, spalt (sal), a known Dll and hth target (Dong et al., 2000), and spalt-related (salr; adjacent and homologous genes with similar expression patterns) are expressed in identical circular patterns in the antennal disc (Barrio et al., 1999; Wagner-Bernholz et al., 1991) and only expressed at low levels in the leg imaginal disc, proximal to the presumptive leg (Fig. 3G). Another target is a bHLH-PAS encoding gene, spineless (ss), a homolog of the mammalian dioxin receptor gene (Duncan et al., 1998). As with Dll and hth loss-of-function mutants, loss of ss also results in antenna to leg transformations (Balkaschina, 1929; Burgess and Duncan, 1990; Struhl, 1982) (Fig. 1D). Dll is required for the antennal expression of ss (Duncan et al., 1998). Also, loss of 1967 Development 129, 1967-1974 (2002) Printed in Great Britain © The Company of Biologists Limited 2002 DEV7937