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The Drosophila proboscis is specified by two Hox genes, proboscipedia and Sex combs reduced, via repression of leg and antennal appendage genes

Arhat Abzhanov^*, Stacy Holtzman^* and Thomas C. Kaufman

Howard Hughes Medical Institute, Department of Biology, Indiana University, Bloomington, IN 47405, USA
^* These authors contributed equally to this work

Author for correspondence (e-mail: kaufman{at}bio.indiana.edu)

Accepted April 23, 2001

The proboscis is one of the most highly modified appendages in Drosophila melanogaster. However, the phenotypes of proboscipedia (pb) mutants, which transform the proboscis into leg or antenna, indicate a basic homology among these limbs. Recent genetic studies have revealed a developmental system for patterning appendages and identified several genes required for limb development. Among these are: extradenticle (exd), homothorax (hth), dachshund (dac), Distal-less (Dll) and spalt (sal). These limb genes have not been well studied in wild-type mouthparts and their role if any in this appendage is not well understood. Here we demonstrate that the homeotic gene products Proboscipedia (Pb) and Sex combs reduced (Scr) regulate the limb genes in the labial disc to give rise to a unique type of appendage, the proboscis. Pb inhibits exd, dac and sal expression and downregulates Dll. This observation explains the ability of Pb to inhibit the effects of ectopically expressed trunk Hox genes in the proboscis, to suppress leg identity in the trunk and to transform antenna to maxillary palp. Scr suppresses sal expression and also downregulates Dll in the labial discs; discs mutant for both pb and Scr give rise to complete antennae, further demonstrating appendage homology. In the labial disc, Pb positively regulates transcription of Scr, whereas in the embryo, Scr positively regulates pb. Additionally, our results suggests a revised fate map of the labial disc. We conclude that the proboscis constitutes a genetically distinct type of appendage whose morphogenesis does not require several important components of leg and/or antennal patterning systems, but retains distal segmental homology with these appendages.

Key words: Drosophila, Proboscis, Labial disc, Homeotic, dachshund, extradenticle, Distal-less, spalt, proboscipedia, Sex combs reduced

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