Abstract
The formation of photoreceptor cells (PRCs) in Drosophila serves as a paradigm for understanding neuronal determination and differentiation. During larval stages, a precise series of sequential inductive processes leads to the recruitment of eight distinct PRCs (R1–R8)1. But, final photoreceptor differentiation, including rhabdomere morphogenesis and opsin expression, is completed four days later, during pupal development2,3. It is thought that photoreceptor cell fate is irreversibly established during larval development, when each photoreceptor expresses a particular set of transcriptional regulators and sends its projection to different layers of the optic lobes. Here, we show that the spalt (sal) gene complex4,5,6,7 encodes two transcription factors that are required late in pupation for photoreceptor differentiation. In the absence of the sal complex, rhabdomere morphology and expression of opsin genes in the inner PRCs R7 and R8 are changed to become identical to those of outer R1–R6 PRCs. However, these cells maintain their normal projections to the medulla part of the optic lobe, and not to the lamina where outer PRCs project. These data indicate that photoreceptor differentiation occurs as a two-step process. First, during larval development, the photoreceptor neurons become committed and send their axonal projections to their targets in the brain. Second, terminal differentiation is executed during pupal development and the photoreceptors adopt their final cellular properties.
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
Dominguez, M., Wasserman, J. D. & Freeman, M. Multiple functions of the EGF receptor in Drosophila eye development. Curr. Biol. 8, 1039–1048 (1998).
Perry, M. M. Further studies on the development of the eye of Drosophila melanogaster. I. The ommatidia. J. Morphol. 124, 227–248 (1968).
Cagan, R. L. & Ready, D. F. The emergence of order in the Drosophila pupal retina. Dev. Biol. 136, 346–362 (1989).
Kuhnlein, R. P. et al. Spalt encodes an evolutionarily conserved zinc finger protein of novel structure which provides homeotic gene function in the head and tail region of the Drosophila embryo. EMBO J. 13, 168–179 (1994).
de Celis, J. F., Barrio, R. & Kafatos, F. C. A gene complex acting downstream of dpp in Drosophila wing morphogenesis. Nature 381, 421–442 (1996).
Rusten, T. E. et al. Spalt modifies EGFR-mediated induction of chordotonal precursors in the embryonic PNS or Drosophila promoting the development of oenocytes. Development 128, 711–722 (2001).
Elstob, P. R., Brodu, V. & Gould, A. P. Spalt-dependent switching between two cell fates that are induced by the Drosophila EGF receptor. Development 128, 723–732 (2001).
Barrio, R., de Celis, J. F., Bolshakov, S. & Kafatos, F. C. Identification of regulatory regions driving the expression of the Drosophila spalt complex at different developmental stages. Dev. Biol. 215, 33–47 (1999).
Mollereau, B. et al. A green fluorescent protein enhancer trap screen in Drosophila photoreceptor cells. Mech. Dev. 93, 151–160 (2000).
Kumar, J. P. & Ready, D. F. Rhodopsin plays an essential structural role in Drosophila photoreceptor development. Development 121, 4359–4370 (1995).
Sheng, G., Thouvenot, E., Schmucker, D., Wilson, D. S. & Desplan, C. Direct regulation of rhodopsin 1 by Pax-6/eyeless in Drosophila: evidence for a conserved function in photoreceptors. Genes Dev. 11, 1122–1131 (1997).
Cadavid, A. L., Ginzel, A. & Fischer, J. A. The function of the Drosophila fat facets deubiquitinating enzyme in limiting photoreceptor cell number is intimately associated with endocytosis. Development 127, 1727–1736 (2000).
Hardie, R. C. in Sensory Physiology 5 (ed. Ottoson, D.) 1–79 (Springer, Heidelberg, 1985).
Papatsenko, D., Sheng, G. & Desplan, C. A new rhodopsin in R8 photoreceptors of Drosophila; evidence for coordinate expression with Rh3 in R7 cells. Development 124, 1665–1673 (1997).
Chou, W. H. et al. Patterning of the R7 and R8 photoreceptor cells of Drosophila: evidence. Development 126, 607–616 (1999).
Stowers, R. S. & Schwarz, T. L. A genetic method for generating Drosophila eyes composed exclusively of mitotic clones of a single genotype. Genetics 152, 1631–1639 (1999).
Kauffmann, R. C., Li, S., Gallagher, P. A., Zhang, J. & Carthew, R. W. Ras1 signaling and transcriptional competence in the R7 cell of Drosophila. Genes Dev. 10, 2167–2178 (1996).
Kimmel, B. E., Heberlein, U. & Rubin, G. M. The homeo domain protein rough is expressed in a subset of cells in the developing Drosophila eye where it can specify photoreceptor cell subtype. Genes Dev. 4, 712–727 (1990).
Begemann, G., Michon, A. M., van der Voorn, L., Wepf, R. & Mlodzik, M. The Drosophila orphan nuclear receptor seven-up requires the Ras pathway for its function in photoreceptor determination. Development 121, 225–235 (1995).
Venkatesh, T. R., Zipursky, S. L. & Benzer, S. Molecular analysis of the development of the compound eye in Drosophila. Trends Neurosci. 8, 251–257 (1985).
Freeman, M. Cell determination strategies in the Drosophila eye. Development 124, 261–270 (1997).
Colley, N. J., Cassill, J. A., Baker, E. K. & Zuker, C. S. Defective intracellular transport is the molecular basis of rhodopsin-dependent dominant retinal degeneration. Proc. Natl Acad. Sci. USA 97, 3070–3074 (1995).
Kumar, J. P., Bowman, J., O'Tousa, J. E. & Rady, D. F. Rhodopsin replacement rescues photoreceptor structure during a critical developmental window. Dev. Biol. 188, 43–47 (1997).
Chang, H. Y. & Ready, D. F. Rescue of photoreceptor degeneration in rhodopsin-null Drosophila mutants by activated Rac1. Science 290, 1978–1980 (2000).
Fortini, M. E. & Rubin, G. M. The optic lobe projection pattern of polarization-sensitive photoreceptor cells in Drosophila melanogaster. Cell Tissue Res. 265, 185–191 (1991).
Furukawa, T., Morrow, E. M. & Cepko, C. L. Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell 91, 531–541 (1997).
Tomlison, A. & Ready, D. F. Cell fate in the Drosophila ommatidium. Dev. Biol. 123, 264–275 (1987).
Porter, J. A. & Montell, C. Distinct roles of the Drosophila ninaC kinase and myosin domains revealed by systematic mutagenesis. J. Cell. Biol. 122, 601–612 (1993).
Chou, W. H. et al. Identification of a novel Drosophila opsin reveals specific patterning of the R7 and R8 photoreceptor cells. Neuron 17, 1101–1115 (1996).
Colley, N. J., Baker, E. K., Stamnes, M. A. & Zuker, C. S. The cyclophilin homolog ninaA is required in the secretory pathway. Cell 67, 255–263 (1991).
Acknowledgements
We are indebted to R. Barrio for her contribution to this work. We thank S. Britt, R. Khünlein, C. Doe, C. Zuker, P. Beaufils and K. Basler for fly stocks and antibodies, the Desplan and Treisman laboratories for support and discussion, and I. Tan for help with ultrathin section analysis. We are also grateful to U. Gaul and M. Mlodzik for allowing us to report unpublished results, J. Treisman for support, and T. Cook and F. Pichaud for comments on the manuscript. We would like to thank Developmental Study Hybridoma Bank for antibodies. B.M. was supported by the Human Frontier Science Program Organization (HFSPO). This work was supported by grants from the National Eye Institute (NEI) to C.D., from HHMI, Research to Prevent Blindness (RPB) and the Retina Research Foundation to N.J.C., and the Dirección General de Investigación from Minesterior de Ciencia y Tecnología (MCYT) to M.D.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Mollereau, B., Dominguez, M., Webel, R. et al. Two-step process for photoreceptor formation in Drosophila. Nature 412, 911–913 (2001). https://doi.org/10.1038/35091076
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/35091076
This article is cited by
-
Uncoupling neuronal death and dysfunction in Drosophila models of neurodegenerative disease
Acta Neuropathologica Communications (2016)
-
Molecular logic behind the three-way stochastic choices that expand butterfly colour vision
Nature (2016)
-
Spalt mediates an evolutionarily conserved switch to fibrillar muscle fate in insects
Nature (2011)
-
Differential expression of the novel oncogene, SALL4, in lymphoma, plasma cell myeloma, and acute lymphoblastic leukemia
Modern Pathology (2006)
-
Control of photoreceptor axon target choice by transcriptional repression of Runt
Nature Neuroscience (2002)
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.
