Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

A rhodopsin in the brain functions in circadian photoentrainment in Drosophila

Abstract

Animals partition their daily activity rhythms through their internal circadian clocks, which are synchronized by oscillating day–night cycles of light. The fruitfly Drosophila melanogaster senses day–night cycles in part through rhodopsin-dependent light reception in the compound eye and photoreceptor cells in the Hofbauer–Buchner eyelet1. A more noteworthy light entrainment pathway is mediated by central pacemaker neurons in the brain. The Drosophila circadian clock is extremely sensitive to light. However, the only known light sensor in pacemaker neurons, the flavoprotein cryptochrome (Cry)2,3, responds only to high levels of light in vitro4. These observations indicate that there is an additional light-sensing pathway in fly pacemaker neurons5. Here we describe a previously uncharacterized rhodopsin, Rh7, which contributes to circadian light entrainment by circadian pacemaker neurons in the brain. The pacemaker neurons respond to violet light, and this response depends on Rh7. Loss of either cry or rh7 caused minor defects in photoentrainment, whereas loss of both caused profound impairment. The circadian photoresponse to constant light was impaired in rh7 mutant flies, especially under dim light. The demonstration that Rh7 functions in circadian pacemaker neurons represents, to our knowledge, the first role for an opsin in the central brain.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Rh7 is a light receptor.
Figure 2: Rh7 contributes to light sensitivity of circadian pacemaker neurons.
Figure 3: Rh7 is a circadian light receptor.
Figure 4: Effects of rh7 mutation on circadian behaviour in response to constant light or constant darkness and on arousal in response to a light pulse.

Similar content being viewed by others

References

  1. Helfrich-Förster, C., Winter, C., Hofbauer, A., Hall, J. C. & Stanewsky, R. The circadian clock of fruit flies is blind after elimination of all known photoreceptors. Neuron 30, 249–261 (2001)

    PubMed  Google Scholar 

  2. Emery, P. et al. Drosophila CRY is a deep brain circadian photoreceptor. Neuron 26, 493–504 (2000)

    CAS  PubMed  Google Scholar 

  3. Stanewsky, R. et al. The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95, 681–692 (1998)

    CAS  PubMed  Google Scholar 

  4. Ozturk, N., Selby, C. P., Annayev, Y., Zhong, D. & Sancar, A. Reaction mechanism of Drosophila cryptochrome. Proc. Natl Acad. Sci. USA 108, 516–521 (2011)

    ADS  CAS  PubMed  Google Scholar 

  5. Szular, J. et al. Rhodopsin 5- and Rhodopsin 6-mediated clock synchronization in Drosophila melanogaster is independent of retinal phospholipase C-β signaling. J. Biol. Rhythms 27, 25–36 (2012)

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Emery, P., Stanewsky, R., Hall, J. C. & Rosbash, M. A unique circadian-rhythm photoreceptor. Nature 404, 456–457 (2000)

    ADS  CAS  PubMed  Google Scholar 

  7. Helfrich-Förster, C. et al. The extraretinal eyelet of Drosophila: development, ultrastructure, and putative circadian function. J. Neurosci. 22, 9255–9266 (2002)

    PubMed  PubMed Central  Google Scholar 

  8. Malpel, S., Klarsfeld, A. & Rouyer, F. Larval optic nerve and adult extra-retinal photoreceptors sequentially associate with clock neurons during Drosophila brain development. Development 129, 1443–1453 (2002)

    CAS  PubMed  Google Scholar 

  9. Sprecher, S. G. & Desplan, C. Switch of Rhodopsin expression in terminally differentiated Drosophila sensory neurons. Nature 454, 533–537 (2008)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  10. Senthilan, P. R. & Helfrich-Förster, C. Rhodopsin 7—the unusual Rhodopsin in Drosophila. PeerJ 4, e2427 (2016)

    PubMed  PubMed Central  Google Scholar 

  11. Zerr, D. M., Hall, J. C., Rosbash, M. & Siwicki, K. K. Circadian fluctuations of period protein immunoreactivity in the CNS and the visual system of Drosophila. J. Neurosci. 10, 2749–2762 (1990)

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Kaneko, M. & Hall, J. C. Neuroanatomy of cells expressing clock genes in Drosophila: transgenic manipulation of the period and timeless genes to mark the perikarya of circadian pacemaker neurons and their projections. J. Comp. Neurol. 422, 66–94 (2000)

    CAS  PubMed  Google Scholar 

  13. Konopka, R. J. & Benzer, S. Clock mutants of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 68, 2112–2116 (1971)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  14. Helfrich-Förster, C. Robust circadian rhythmicity of Drosophila melanogaster requires the presence of lateral neurons: a brain-behavioral study of disconnected mutants. J. Comp. Physiol. A 182, 435–453 (1998)

    PubMed  Google Scholar 

  15. Renn, S. C., Park, J. H., Rosbash, M., Hall, J. C. & Taghert, P. H. A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99, 791–802 (1999)

    CAS  PubMed  Google Scholar 

  16. Yoshii, T., Todo, T., Wülbeck, C., Stanewsky, R. & Helfrich-Förster, C. Cryptochrome is present in the compound eyes and a subset of Drosophila’s clock neurons. J. Comp. Neurol. 508, 952–966 (2008)

    CAS  PubMed  Google Scholar 

  17. Helfrich-Förster, C. et al. Development and morphology of the clock-gene-expressing lateral neurons of Drosophila melanogaster. J. Comp. Neurol. 500, 47–70 (2007)

    PubMed  Google Scholar 

  18. Fogle, K. J., Parson, K. G., Dahm, N. A. & Holmes, T. C. CRYPTOCHROME is a blue-light sensor that regulates neuronal firing rate. Science 331, 1409–1413 (2011)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  19. Sheeba, V., Gu, H., Sharma, V. K., O’Dowd, D. K. & Holmes, T. C. Circadian- and light-dependent regulation of resting membrane potential and spontaneous action potential firing of Drosophila circadian pacemaker neurons. J. Neurophysiol. 99, 976–988 (2008)

    PubMed  Google Scholar 

  20. Fogle, K. J. et al. CRYPTOCHROME-mediated phototransduction by modulation of the potassium ion channel β-subunit redox sensor. Proc. Natl Acad. Sci. USA 112, 2245–2250 (2015)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  21. Dushay, M. S. et al. Phenotypic and genetic analysis of Clock, a new circadian rhythm mutant in Drosophila melanogaster. Genetics 125, 557–578 (1990)

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Kistenpfennig, C., Hirsh, J., Yoshii, T. & Helfrich-Förster, C. Phase-shifting the fruit fly clock without cryptochrome. J. Biol. Rhythms 27, 117–125 (2012)

    PubMed  Google Scholar 

  23. Vinayak, P. et al. Exquisite light sensitivity of Drosophila melanogaster cryptochrome. PLoS Genet. 9, e1003615 (2013)

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Koh, K., Zheng, X. & Sehgal, A. JETLAG resets the Drosophila circadian clock by promoting light-induced degradation of TIMELESS. Science 312, 1809–1812 (2006)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  25. Guo, F., Cerullo, I., Chen, X. & Rosbash, M. PDF neuron firing phase-shifts key circadian activity neurons in Drosophila. eLife 3, e02780 (2014)

    PubMed Central  Google Scholar 

  26. Sheeba, V. et al. Large ventral lateral neurons modulate arousal and sleep in Drosophila. Curr. Biol. 18, 1537–1545 (2008)

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Shang, Y., Griffith, L. C. & Rosbash, M. Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain. Proc. Natl Acad. Sci. USA 105, 19587–19594 (2008)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  28. Siwicki, K. K., Eastman, C., Petersen, G., Rosbash, M. & Hall, J. C. Antibodies to the period gene product of Drosophila reveal diverse tissue distribution and rhythmic changes in the visual system. Neuron 1, 141–150 (1988)

    CAS  PubMed  Google Scholar 

  29. Nitabach, M. N. et al. Electrical hyperexcitation of lateral ventral pacemaker neurons desynchronizes downstream circadian oscillators in the fly circadian circuit and induces multiple behavioral periods. J. Neurosci. 26, 479–489 (2006)

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Blackshaw, S. & Snyder, S. H. Encephalopsin: a novel mammalian extraretinal opsin discretely localized in the brain. J. Neurosci. 19, 3681–3690 (1999)

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Grether, M. E., Abrams, J. M., Agapite, J., White, K. & Steller, H. The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev. 9, 1694–1708 (1995)

    CAS  PubMed  Google Scholar 

  32. Emery, P., So, W. V., Kaneko, M., Hall, J. C. & Rosbash, M. CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell 95, 669–679 (1998)

    CAS  PubMed  Google Scholar 

  33. Dolezelova, E., Dolezel, D. & Hall, J. C. Rhythm defects caused by newly engineered null mutations in Drosophila’s cryptochrome gene. Genetics 177, 329–345 (2007)

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Yamaguchi, S., Wolf, R., Desplan, C. & Heisenberg, M. Motion vision is independent of color in Drosophila. Proc. Natl Acad. Sci. USA 105, 4910–4915 (2008)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  35. Vasiliauskas, D. et al. Feedback from rhodopsin controls rhodopsin exclusion in Drosophila photoreceptors. Nature 479, 108–112 (2011)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  36. O’Tousa, J. E. et al. The Drosophila ninaE gene encodes an opsin. Cell 40, 839–850 (1985)

    PubMed  Google Scholar 

  37. Venken, K. J. et al. Versatile P[acman] BAC libraries for transgenesis studies in Drosophila melanogaster. Nat. Methods 6, 431–434 (2009)

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Gong, W. J. & Golic, K. G. Ends-out, or replacement, gene targeting in Drosophila. Proc. Natl Acad. Sci. USA 100, 2556–2561 (2003)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  39. Lee, Y. & Montell, C. Drosophila TRPA1 functions in temperature control of circadian rhythm in pacemaker neurons. J. Neurosci. 33, 6716–6725 (2013)

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Jang, A. R., Moravcevic, K., Saez, L., Young, M. W. & Sehgal, A. Drosophila TIM binds importin α1, and acts as an adapter to transport PER to the nucleus. PLoS Genet. 11, e1004974 (2015)

    PubMed  PubMed Central  Google Scholar 

  41. Zuker, C. S., Cowman, A. F. & Rubin, G. M. Isolation and structure of a rhodopsin gene from D. melanogaster. Cell 40, 851–858 (1985)

    CAS  PubMed  Google Scholar 

  42. Montell, C., Jones, K., Zuker, C. & Rubin, G. A second opsin gene expressed in the ultraviolet-sensitive R7 photoreceptor cells of Drosophila melanogaster. J. Neurosci. 7, 1558–1566 (1987)

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Zuker, C. S., Montell, C., Jones, K., Laverty, T. & Rubin, G. M. A rhodopsin gene expressed in photoreceptor cell R7 of the Drosophila eye: homologies with other signal-transducing molecules. J. Neurosci. 7, 1550–1557 (1987)

    CAS  PubMed  PubMed Central  Google Scholar 

  44. 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)

    CAS  PubMed  Google Scholar 

  45. 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)

    CAS  PubMed  Google Scholar 

  46. Chou, W. H. et al. Patterning of the R7 and R8 photoreceptor cells of Drosophila: evidence for induced and default cell-fate specification. Development 126, 607–616 (1999)

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank A. Sehgal, M. Rosbash, M. Wu and P. Emery for fly stocks; A. Sehgal and S. Britt for antibodies; and E. Guzman, H. Zhou and the Next Generation Sequencing Core at the UCSB Biological Nanostructures Laboratory for help with the RNA-seq. This work was supported by grants to C.M. from the National Eye Institute (EY008117) and the National Institute on Deafness and other Communication Disorders (DC007864), and to T.C.H. from National Institute of General Medical Sciences (GM102965 and GM107405).

Author information

Authors and Affiliations

Authors

Contributions

J.D.N., T.C.H. and C.M. designed the study. J.D.N. and L.S.B. performed experiments, and all authors analysed the data. J.D.N. and C.M. wrote the manuscript with input from T.C.H. and L.S.B.

Corresponding author

Correspondence to Craig Montell.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Reviewer Information Nature thanks C. Desplan, R. Stanewsky and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data figures and tables

Extended Data Figure 1 Circadian photoentrainment in flies lacking cryptochrome and proteins required for phototransduction in the compound eye.

ag, Average actograms exhibited by flies of the indicated genotypes maintained under L–D for 4 days and then released to constant darkness. h, Summary of circadian rhythmicity of flies in ag. Rhythm strength of a fly was measured as p − s.

Extended Data Figure 2 Rh7 is an extraretinal opsin.

a, Phylogenetic tree constructed with protein sequences corresponding to the indicated opsins. The full name for A. gambiae OP10 is GPROP10 (VectorBase). b, Cartoon showing a longitudinal view of the main structures in the Drosophila visual system, including the retina, lamina and medulla. The blue units represent ommatidia, which comprise eight photoreceptor cells (R1–8) and support cells. c, Cartoon showing the photoreceptor cells in a single ommatidium. The six outer photoreceptor cells (R1–R6) are represented in blue and express Rh136,41. The central R7 photoreceptor cell (purple) expresses Rh3 or Rh442,43, while the R8 photoreceptor cell (green) expresses Rh5 or Rh644,45,46. d, A wild-type retina stained with anti-Rh7 (red) and anti-Rh3 (green). e, A wild-type retina stained with anti-Rh7 (red) and anti-Rh5 (green). Scale bars, 30 μm. No Rh7-positive staining was detected in the retina. f, Generation of rh71 by homologous recombination. Shown are cartoons of the wild-type rh7 locus (top) and the genomic organization of the rh71 allele (bottom). The triangles (P1–P4) indicate the primers used to verify the rh71 mutation. g, Confirmation of the rh71 mutation by PCR. We prepared genomic DNA from control (w1118) and rh71 flies and performed PCR using the P1–P2 and P3–P4 primer pairs. The positions of DNA markers (kb) are indicated to the right. See Supplementary Information for the raw images of the PCR gels. h, ERG amplitudes of control and rh71 flies using 2-s white light pulses of the indicated intensities. Error bars indicate s.e.m., n = 4. i–m, ERGs from flies of the indicated genotypes. The event markers below the ERGs indicate light pulses. i, Control flies. j, rh71 flies. k–m, Testing for rescue of the reduced ERG amplitude and loss of on- and off-transients in ninaEI17 flies with an rh7+ transgene. k, Control flies. l, ninaEI17 (rh1 mutant). m, ninaEI17 fly expressing UAS–rh7 in R1–R6 cells under control of rh1–Gal4 (ninaEI17, rh1>rh7).

Extended Data Figure 3 Expression of Rh7 in non-Cry neurons in the dorsal brain.

a, Cartoon of a fly brain showing different groups of clock neurons. The boxed areas indicate locations of two groups of Rh7-positive cells. b, rh71 brain stained with anti-Rh7. ce, Double labelling of the dorsal region of the brain with a Cry neuron reporter (cry–Gal4E13>UAS–mCherry–NLS) and anti-Rh7. c, Anti-Rh7. d, Anti-mCherry. e, Merge of c and d. f, Control brain stained with anti-Rh7. g, Control brain stained with anti-PDF. h, pdf-Gal4>rh7RNAi brain stained with anti-Rh7. i, pdf-Gal4>rh7RNAi brain stained with anti-PDF. Scale bars: be, 20 μm; fi, 10 μm.

Extended Data Figure 4 Actograms showing representative behaviour of control and mutant flies before and after a 5-min light pulse at the indicated ZT.

Red dots connected by dashed red lines indicate evening peaks before and after the light pulse. Each yellow arrow indicates exposure to a 5-min ~600 lx LED light pulse.

Extended Data Figure 5 Circadian responses to constant light and light-dependent arousal in rh71 flies.

a, b, Flies of the indicated genotypes were entrained under L–D cycles and subsequently released to constant ~400 lx light (L–L). c, d, Flies of the indicated genotypes were entrained under L–D cycles and subsequently released to constant ~10 lx light (L–L). e, Quantification of the effect of a 5-min white light pulse on arousal. Arousal was quantified as increases in total bin crosses during the 5-min light stimulation compared to the total bin crosses during the 5 min before light stimulation. f, Quantification of the time required to reach maximum activity after white light stimulation. g, h, Quantification of the effects on arousal of a 5-min exposure to red (625 nm) (g) or violet (405 nm) LED lights (h). Error bars indicate s.e.m. One-away ANOVA (Kruskal–Wallis test) followed by Dunn’s test. *P < 0.05, **P < 0.01. Number of flies tested: norpAP24, n = 16; other genotypes, n = 24.

Extended Data Figure 6 Effects of multiple light input pathways on circadian behaviour.

a, b, Actograms showing rhythmic and arrhythmic rh71 cry01 double mutants. The flies were entrained under L–D cycles and subsequently released to constant darkness. c, Percentages of rhythmic and arrhythmic flies. Fisher’s exact test, **P < 0.01. Number of flies tested: control, n = 16; other genotypes, n = 30. dh, Circadian behaviour of gl60j and rh71 gl60j double mutant flies. The flies were entrained to L–D cycles for 4 days and subsequently released to constant darkness. d, Percentages of rhythmic and arrhythmic flies. eh, Average actograms showing the activities of flies of the indicated genotypes. Number of flies tested: control, n = 46; rh71, n = 34; gl60j, n = 38; rh71 gl60j, n = 40. i, Phase response of the indicated genotypes to 5-min white light stimulation at ZT22. Error bars indicate s.e.m. One-way ANOVA (Kruskal–Wallis test) followed by Dunn’s test. **P < 0.01. Flies tested: control, n = 54; rh71, n = 49; gl60j, n = 53; rh71 gl60j, n = 57.

Extended Data Figure 7 Rescue of the rh71 cryb photoentrainment defect by expression of rh7 in pacemaker neurons.

ac, Actograms of control flies and rh71 cryb flies harbouring only the UAS–rh7 or pdf–Gal4 transgenes. Number of flies tested: control, n = 16; UAS–rh7/+; rh71 cryb, n = 52; pdf–Gal4/+; rh71 cryb, n = 21. df, Actograms of rh71 cryb flies expressing UAS–rh7 in pacemaker neurons under the control of tim–Gal4 or pdf–Gal4 as indicated. Number of flies tested: UAS–rh7/tim–Gal4;rh71 cryb, n = 37; UAS–rh7/pdf–Gal4; rh71 cryb, n = 23; UAS–rh7–flag/pdf–Gal4;rh71 cryb, n = 21. g, Percentages of rhythmic and arrhythmic flies of the indicated genotypes. Fisher’s exact test, *P < 0.05.

Extended Data Figure 8 Rescue of rh71 cryb photoentrainment defect by expression of other fly rhodopsins.

af, Controls showing actograms of rh71 cryb flies harbouring UAS–rhodopsin transgenes only, and of rh71 cryb flies expressing the indicated rhodopsin genes in pacemaker neurons under the control of pdf–Gal4. Number of flies tested: UAS–rh3/+;rh71 cryb, n = 56; UAS–rh4/+;rh71 cryb, n = 46; UAS–rh5/+;rh71 cryb, n = 24; UAS–rh3/pdf–Gal4;rh71 cryb, n = 64; UAS–rh4/pdf–Gal4;rh71 cryb, n = 25; UAS–rh5/pdf–Gal4;rh71 cryb, n = 16. g, Percentages of rhythmic and arrhythmic flies of the indicated genotypes. Fisher’s exact test, *P < 0.05, ***P < 0.001.

Extended Data Figure 9 Per oscillates in control, rh71, cryb and rh71 cryb flies.

a, d, g, j, Flies of the indicated genotypes were entrained under L–D cycles for 4 days and the brains were dissected on the 5th day. The ZT times indicate when the brains were fixed and dissected for staining with anti-Per (Per, upper rows, red) and anti-PDF (PDF, lower rows, green) as indicated. At least one s-LNV (s) and one l-LNV (l) are labelled in the images obtained at each ZT to facilitate identification of LNVs. Scale bars, 10 μm. b, c, e, f, h, i, k, l, Quantification of relative Per levels in s-LNvs and L-LNVs of flies of the indicated genotypes. The image quantification was performed using ImageJ. The y axes indicate relative Per intensities. The Per intensities in ZT2 of the control flies were designated as 100. For control flies, ZT10, n = 6; ZT22, n = 8; n = 5 for all other time points. For rh71, ZT2, n = 9; ZT6, n = 8; ZT10, n = 6; ZT14, n = 8; ZT18, n = 8; ZT22, n = 7. For cryb, ZT2, n = 8; ZT6, n = 9; ZT10, n = 8; ZT14, n = 7; ZT18, n = 10; ZT22, n = 8. For rh71 cryb, n = 5 for all time points. Error bars indicate s.e.m.

Extended Data Figure 10 Knockdown of plc21C in PDF-positive neurons impaired circadian phase response.

a, Quantitative real-time PCR analysis of plc21C mRNA using RNA prepared from whole adults. The plc21C expression levels in each sample were normalized using rp49 expression. The control was w1118. Centre values indicate the average and error bars indicate s.e.m. One-away ANOVA (Kruskal–Wallis test) followed by Dunn’s test. **P < 0.01. b, Phase response of the indicated genotypes to 5 min white light stimulation at ZT22. One-away ANOVA (Kruskal–Wallis test) followed by Dunn’s test. **P < 0.01. pdf–Gal4/+, n = 32; plc21C–RNAi01211/+, n = 31; pdf–Gal4>plc21C–RNAi01211, n = 37; plc21C–RNAi01210/+, n = 15; pdf–Gal4>plc21C–RNAi01210, n = 32. Error bars indicate s.e.m. cg, Examples of behaviour before and after the 5-min light pulse. The yellow arrows indicate the times of the 5-min white light pulses (~600 lx). The red dots connected by dashed red lines indicate the evening peaks before and after the light pulse.

Supplementary information

Supplementary Information

This file contains the raw images of the PCR gels. (PDF 141 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ni, J., Baik, L., Holmes, T. et al. A rhodopsin in the brain functions in circadian photoentrainment in Drosophila. Nature 545, 340–344 (2017). https://doi.org/10.1038/nature22325

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature22325

This article is cited by

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.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing