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Switch of rhodopsin expression in terminally differentiated Drosophila sensory neurons

Abstract

Specificity of sensory neurons requires restricted expression of one sensory receptor gene and the exclusion of all others within a given cell. In the Drosophila retina, functional identity of photoreceptors depends on light-sensitive Rhodopsins (Rhs). The much simpler larval eye (Bolwig organ) is composed of about 12 photoreceptors, eight of which are green-sensitive (Rh6) and four blue-sensitive (Rh5)1. The larval eye becomes the adult extraretinal ‘eyelet’ composed of four green-sensitive (Rh6) photoreceptors2,3. Here we show that, during metamorphosis, all Rh6 photoreceptors die, whereas the Rh5 photoreceptors switch fate by turning off Rh5 and then turning on Rh6 expression. This switch occurs without apparent changes in the programme of transcription factors that specify larval photoreceptor subtypes. We also show that the transcription factor Senseless (Sens) mediates the very different cellular behaviours of Rh5 and Rh6 photoreceptors. Sens is restricted to Rh5 photoreceptors and must be excluded from Rh6 photoreceptors to allow them to die at metamorphosis. Finally, we show that Ecdysone receptor (EcR) functions autonomously both for the death of larval Rh6 photoreceptors and for the sensory switch of Rh5 photoreceptors to express Rh6. This fate switch of functioning, terminally differentiated neurons provides a novel, unexpected example of hard-wired sensory plasticity.

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Figure 1: Transformation of the larval eye into the adult eyelet.
Figure 2: Larval Rh5 photoreceptors give rise to the eyelet and express Rh5 photoreceptor markers.
Figure 3: EcR expression and activity in larval photoreceptors before metamorphosis.
Figure 4: EcR is required autonomously for the fate switch of Rh5 photoreceptors and apoptosis of Rh6 photoreceptors.

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Acknowledgements

We thank H. Bellen, A. H. Brand, S. Britt, T. Cook, the Developmental Studies Hybridoma Bank, F. Hirth, the Kyoto Stock Center, K. Matthews, M. Mlodzik, B. Mollerau, F. Pichaud, H. Reichert, C. Thummel and J. Urban for fly stocks and antibodies. We also thank J. Blau, R. J. Johnston, A. Keene and D. Vasiliauskas for discussion and comments on the manuscript. This work was funded by grant EY013010 from the National Eye Institute/National Institutes of Health to C.D., the Swiss National Science Foundation, the Novartis Foundation and the Janggen-Pöhn Stiftung (to S.G.S.) and conducted in a facility constructed with the support of a Research Facilities Improvement Grant C06 RR-15518-01 from the National Center for Research Resources, National Institutes of Health.

Author Contributions S.G.S. performed the experimental work and analysed the data. C.D. and S.G.S. designed the experiments and wrote the paper.

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Correspondence to Claude Desplan.

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Sprecher, S., Desplan, C. Switch of rhodopsin expression in terminally differentiated Drosophila sensory neurons. Nature 454, 533–537 (2008). https://doi.org/10.1038/nature07062

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