Abstract
THE Drosophila peripheral nervous system comprises four major types of sensory element: external sense organs (such as mechano-sensory bristles), chordotonal organs (internal stretch receptors), multiple dendritic neurons, and photoreceptors. During development, the selection of neural precursors for external sense organs requires the proneural genes of the achaete–scute complex, which encode basic-helix–loop–helix transcription factors1–3. These genes do not, however, control precursor selection for chordotonal organs or photoreceptors4,5, raising the question of whether other proneural genes exist6 or a different mechanism of neurogenesis operates. Here we show that atonal (ato), originally isolated as a proneural gene for chordotonal organs7, is also the proneural gene for photo-receptors. Pattern formation in the Drosophila eye involves a succession of cell fate specifications. Of the eight photoreceptors within each ommatidium of the compound eye, the photoreceptor R8 is the first to appear in the eye imaginal disc, right behind the mor-phogenetic furrow8–10. The appearance of other photoreceptors (Rl–7) follows in a defined sequence that is thought to arise by induction from R8 (refs 8, 9, 11, 12). We find that photoreceptor formation requires the function of atonal at the morphogenetic furrow and that atonal is specifically required for R8 selection. Formation of other photoreceptors does not directly require atonal function, but does depend on R8 selection by atonal. Thus, photo-receptors are selected by two mechanisms: R8 by a proneural mechanism, and Rl–7 by local recruitment.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Ghysen, A. & Dambly-Chaudière, C. Trends Genet. 56, 251–255 (1989).
Campuzano, S. & Modolell, J. Trends Genet. 8, 202–208 (1992).
Ghysen, A., Dambly-Chaudière, C., Jan, L. Y. & Jan, Y. N. Genes Dev. 7, 723–733 (1993).
Dambly-Chaudière, C. & Ghysen, A. Genes Dev. 1, 297–306 (1987).
Jiménez, F. & Campos-Ortega, J. A. J. Neurogen. 4, 179 (1987).
Basler, K. & Hafen, E. BioEssays 13, 621–631 (1991).
Jarman, A. P., Grau, Y., Jan, L. Y. & Jan, Y. N. Cell 73, 1307–1321 (1993).
Tomlinson, A. & Ready, D. F. Devl Biol. 120, 366–376 (1987).
Ready, D. F. Trends Neurosci. 12, 102–110 (1989).
Baker, N. E., Mlodzik, M. & Rubin, G. M. Science 250, 1370–1377 (1990).
Banerjee, U. & Zipursky, S. L. Neuron 4, 177–187 (1990).
Rubin, G. R. Trends Genet. 7, 372–377 (1991).
Baker, N. E. & Rubin, G. M. Nature 340, 150–153 (1989).
Zipursky, S. L., Venkatesh, T. R., Teplow, D. B. & Benzer, S. Cell 36, 15–26 (1984).
Mlodzic, M., Baker, N. E. & Rubin, G. M. Genes Dev. 4, 1848–1861 (1990).
Heberlein, U., Wolff, T. & Rubin, G. M. Cell 75, 913–926 (1993).
Ma, C., Zhou, Y., Beachy, P. A. & Moses, K. Cell 75, 927–938 (1993).
Heberlein, U., Hariharan, I. K. & Rubin, G. M. Devl Biol. 160, 51–63 (1993).
Cagan, R. L. & Ready, D. L. Genes Dev. 3, 1099–1112 (1989).
Karpilow, J., Kolodkin, A., Bork, T. & Venkatesh, T. Genes Dev. 3, 1834–1844 (1989).
Mclver, S. B. in Comprehensive Insect Physiology, Biochemistry and Pharmacology Vol. 6 (eds Gilbert, L. I. & Kerkut, D. A.) (Pergamon, New York, 1985).
Meyerowitz, E. M. & Kankel, D. R. Devl Biol. 62, 112–142 (1978).
Fischbach, K. F. & Technau G. Devl Biol. 104, 219–239 (1984).
Lindsley, D. L. & Zimm, G. G. in Tne Genome of Drosophila melangoaster (Academic, San Diego, 1992).
Brand, A. H. & Perrimon, N. Development 118, 401–415 (1993).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Jarman, A., Grell, E., Ackerman, L. et al. atonal is the proneural gene for Drosophila photoreceptors. Nature 369, 398–400 (1994). https://doi.org/10.1038/369398a0
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/369398a0
This article is cited by
-
GFI1 regulates hair cell differentiation by acting as an off-DNA transcriptional co-activator of ATOH1, and a DNA-binding repressor
Scientific Reports (2022)
-
Differential regulation of mammalian and avian ATOH1 by E2F1 and its implication for hair cell regeneration in the inner ear
Scientific Reports (2021)
-
Motif 1 Binding Protein suppresses wingless to promote eye fate in Drosophila
Scientific Reports (2020)
-
Homeostatic maintenance and age-related functional decline in the Drosophila ear
Scientific Reports (2020)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.