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Feedback from rhodopsin controls rhodopsin exclusion in Drosophila photoreceptors

Abstract

Sensory systems with high discriminatory power use neurons that express only one of several alternative sensory receptor proteins. This exclusive receptor gene expression restricts the sensitivity spectrum of neurons and is coordinated with the choice of their synaptic targets1,2,3. However, little is known about how it is maintained throughout the life of a neuron. Here we show that the green-light sensing receptor rhodopsin 6 (Rh6) acts to exclude an alternative blue-sensitive rhodopsin 5 (Rh5) from a subset of Drosophila R8 photoreceptor neurons4. Loss of Rh6 leads to a gradual expansion of Rh5 expression into all R8 photoreceptors of the ageing adult retina. The Rh6 feedback signal results in repression of the rh5 promoter and can be mimicked by other Drosophila rhodopsins; it is partly dependent on activation of rhodopsin by light, and relies on Gαq activity, but not on the subsequent steps of the phototransduction cascade5. Our observations reveal a thus far unappreciated spectral plasticity of R8 photoreceptors, and identify rhodopsin feedback as an exclusion mechanism.

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Figure 1: Rh6 acts to repress Rh5 expression in yR8 photoreceptors.
Figure 2: Rh6 represses transcription of the rh5 gene.
Figure 3: Mutation of rh6 does not lead to change in yR8 cell identity.
Figure 4: Part of the phototransduction pathway is required to maintain repression of Rh5.

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Acknowledgements

We thank J. Blau, B. Collins, M. Cols, T. Erclik, S.H. Fuss, D. Jukam, J.P. Kumar, E. Laufer, H.-S. Li, B. Minke, C. Montell, F. Pichaud, J. Rister and A. Tomlinson for suggestions and comments on the manuscript, V. Douard for help with qRT–PCR, J. Goodness for help identifying rh6fs allele, S.G. Britt, P.J. Dolph, P.R. Hiesinger, F. Pichaud, N. Pinal, D.F. Ready, C.S. Zuker, and the Bloomington Drosophila Stock Center for flies or antibodies. This work was funded by the National Institutes of Health R01EY13012 to C.D. and F32EY016309 to D.V.

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D.V., E.O.M. and C.D. conceived the experiments; D.V. and E.O.M. designed and performed experiments in adult flies; S.G.S. designed and performed experiments in larvae; K.B. performed RNAi experiments; R.J.J., P.L., N.V. and A.C. contributed reagents; D.V. and C.D. wrote the paper.

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Correspondence to Claude Desplan.

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Vasiliauskas, D., Mazzoni, E., Sprecher, S. et al. Feedback from rhodopsin controls rhodopsin exclusion in Drosophila photoreceptors. Nature 479, 108–112 (2011). https://doi.org/10.1038/nature10451

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