atonal is a proneural gene for a subset of olfactory sense organs in Drosophila

BACKGROUND: The antenna of the adult fruit fly, Drosophila melanogaster, is covered with three morphologically distinct types of olfactory sense organs. In addition, mechano- and hygro-sensitive receptors are also present on its surface. While much has been learnt about the development of peripheral nervous system in Drosophila, the mechanisms underlying the development of olfactory sensilla are just beginning to be unraveled. The antennal sense organs have several properties that make them distinct from other sense organs. While each sensillum type is arranged in a well-defined region of the antenna, the position of an individual sensillum is not fixed. The development of these sense organs appears to combine an initial step of cell recruitment, as in photoreceptors, followed by cell lineage mechanisms, as in the development of other external sense organs. The earliest step in development, the selection of a sensory organ precursor, involves the interaction of proneural and neurogenic genes. The proneural gene for the antennal sense organs has been elusive so far. RESULTS: We show that the basic helix-loop-helix (bHLH) transcription factor encoded by atonal (ato) is a proneural gene for one morphological type of olfactory sensilla on the antenna and for all the olfactory sensilla on the maxillary palp. Loss of function and overexpression experiments together reveal that ato is both necessary and sufficient to specify these sensilla. Immunohistochemical experiments show that Ato expresses in a dynamic pattern in the developing antennal disc. CONCLUSIONS: Our results demonstrate that ato acts solely in the specification of antennal sensilla coeloconica. This along with our previous observation that the AS-C genes do not function in antenna allows us to suggest that other proneural genes must operate in the specification of sensilla basiconica and trichoidea. Our experiment involving overexpression of extramacrochaetae, a negative regulator of bHLH encoding genes, results in a significant reduction in the number of all three types of antennal sensilla. This suggests that the unidentified proneural gene(s) possibly encode bHLH factors.