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PDF-modulated visual inputs and cryptochrome define diurnal behavior in Drosophila

Nature Neuroscience volume 12, pages 1431–1437 (2009)Cite this article

Abstract

Morning and evening circadian oscillators control the bimodal activity of Drosophila in light-dark cycles. The lateral neurons evening oscillator (LN-EO) is important for promoting diurnal activity at dusk. We found that the LN-EO autonomously synchronized to light-dark cycles through either the cryptochrome (CRY) that it expressed or the visual system. In conditions in which CRY was not activated, flies depleted for pigment-dispersing factor (PDF) or its receptor lost the evening activity and displayed reversed PER oscillations in the LN-EO. Rescue experiments indicated that normal PER cycling and the presence of evening activity relied on PDF secretion from the large ventral lateral neurons and PDF receptor function in the LN-EO. The LN-EO thus integrates light inputs and PDF signaling to control Drosophila diurnal behavior, revealing a new clock-independent function for PDF.

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Figure 1: Characterization of the LN-MO and LN-EO.
Figure 2: Light entrainment of flies lacking either CRY or the visual system.
Figure 3: Light-dark activity and light entrainment of PDF-depleted flies.
Figure 4: Oscillations of PER levels in the clock neurons in the absence of PDF and/or CRY.
Figure 5: Averaged locomotor activity profiles of rescued pdf0cryb and pdfr mutants.
Figure 6: Light-dark activity of rescued pdf0cryb mutants and model for the new PDF function.

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Acknowledgements

We thank M. Boudinot for the FaasX software and ImageJ plugins, G. Levesque for helping with the behavioral setup, O. Lenoir and C. Lancelin for preliminary behavioral experiments and C. Vias for her help with dissections. We thank J. Champagnat for his strong support and M. Rosbash, Y. Shang and the members of the Rouyer laboratory for their comments on the manuscript. We are grateful to M. Ahmad, J. Hall, J. Kim, M. Rosbash, R. Stanewsky, P. Taghert and R. Ueda for providing material, stocks and reagents. This work was supported by Agence Nationale de la Recherche 'Neurosciences, neurologie et psychiatrie' and the European Union 6th framework project 'EUCLOCK'. P.C. was supported by EUCLOCK, M.P. by Ministère de l'Enseignement Supérieur et de la Recherche and Fondation pour le Recherche Médicale, B.R. by Ministère de l'Enseignement Supérieur et de la Recherche and Association pour la Recherche sur le Cancer, and F.R. by Institut National de la Santé et des Etudes et Recherches Médicale.

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  1. Institut de Neurobiologie Alfred Fessard, Centre National de la Recherche Scientifique (UPR 2216), Gif-sur-Yvette, France

    Paola Cusumano, André Klarsfeld, Elisabeth Chélot, Marie Picot, Benjamin Richier & François Rouyer

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  1. Paola Cusumano
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Contributions

P.C., A.K. and F.R. conceived and designed the experiments. P.C., A.K. and E.C. performed the experiments and analyzed the data. M.P. contributed to behavioral analyses. B.R. contributed to microscopy analysis. P.C., A.K. and F.R. wrote the paper.

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Correspondence to François Rouyer.

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Cusumano, P., Klarsfeld, A., Chélot, E. et al. PDF-modulated visual inputs and cryptochrome define diurnal behavior in Drosophila. Nat Neurosci 12, 1431–1437 (2009). https://doi.org/10.1038/nn.2429

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