Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall

Article metrics

Abstract

Photoreceptors for visual perception, phototaxis or light avoidance are typically clustered in eyes or related structures such as the Bolwig organ of Drosophila larvae. Unexpectedly, we found that the class IV dendritic arborization neurons of Drosophila melanogaster larvae respond to ultraviolet, violet and blue light, and are major mediators of light avoidance, particularly at high intensities. These class IV dendritic arborization neurons, which are present in every body segment, have dendrites tiling the larval body wall nearly completely without redundancy. Dendritic illumination activates class IV dendritic arborization neurons. These novel photoreceptors use phototransduction machinery distinct from other photoreceptors in Drosophila and enable larvae to sense light exposure over their entire bodies and move out of danger.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Photoreceptors in addition to Bolwig organs contribute to photoavoidance.
Figure 2: Light activates class IV dendritic arborization neurons.
Figure 3: Cell-autonomous activation of class IV dendritic arborization neurons by light.
Figure 4: Gr28b and TrpA1 are essential for class IV dendritic arborization neuron light responses.
Figure 5: Class IV dendritic arborization neurons are the extra-ocular photoreceptors that contribute to light avoidance.

References

  1. 1

    Fu, Y., Liao, H. W., Do, M. T. & Yau, K. W. Non-image-forming ocular photoreception in vertebrates. Curr. Opin. Neurobiol. 15, 415–422 (2005)

  2. 2

    Yau, K. W. & Hardie, R. C. Phototransduction motifs and variations. Cell 139, 246–264 (2009)

  3. 3

    Steven, D. M. The dermal light sense. Biol. Rev. Camb. Philos. Soc. 38, 204–240 (1963)

  4. 4

    Millott, N. The dermal light sense. Symp. Zool. Soc. Lond. 23, 1–36 (1968)

  5. 5

    Yoshida, M. Extraocular photoreception. In Handbook of Sensory Physiology Vol. 7/6A, 581–640 (Springer, 1979)

  6. 6

    Halford, S. et al. VA opsin-based photoreceptors in the hypothalamus of birds. Curr. Biol. 19, 1396–1402 (2009)

  7. 7

    Phillips, J. B., Deutschlander, M. E., Freake, M. J. & Borland, S. C. The role of extraocular photoreceptors in newt magnetic compass orientation: parallels between light-dependent magnetoreception and polarized light detection in vertebrates. J. Exp. Biol. 204, 2543–2552 (2001)

  8. 8

    Ward, A., Liu, J., Feng, Z. & Xu, X. Z. Light-sensitive neurons and channels mediate phototaxis in C. elegans . Nature Neurosci. 11, 916–922 (2008)

  9. 9

    Edwards, S. L. et al. A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans . PLoS Biol. 6, e198 (2008)

  10. 10

    Liu, J. et al. elegans phototransduction requires a G protein-dependent cGMP pathway and a taste receptor homolog. Nature Neurosci. 13, 715–722 (2010)

  11. 11

    Sawin-McCormack, E. P., Sokolowski, M. B. & Campos, A. R. Characterization and genetic analysis of Drosophila melanogaster photobehavior during larval development. J. Neurogenet. 10, 119–135 (1995)

  12. 12

    Mazzoni, E. O., Desplan, C. & Blau, J. Circadian pacemaker neurons transmit and modulate visual information to control a rapid behavioral response. Neuron 45, 293–300 (2005)

  13. 13

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

  14. 14

    Willson, R. C., Gulkis, S., Janssen, M., Hudson, H. S. & Chapman, G. A. Observations of solar irradiance variability. Science 211, 700–702 (1981)

  15. 15

    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)

  16. 16

    Hay, B. A., Maile, R. & Rubin, G. M. P element insertion-dependent gene activation in the Drosophila eye. Proc. Natl Acad. Sci. USA 94, 5195–5200 (1997)

  17. 17

    Nakai, J., Ohkura, M. & Imoto, K. A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein. Nature Biotechnol. 19, 137–141 (2001)

  18. 18

    Wang, J. W., Wong, A. M., Flores, J., Vosshall, L. B. & Axel, R. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112, 271–282 (2003)

  19. 19

    Tian, L. et al. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nature Methods 6, 875–881 (2009)

  20. 20

    Ueda, A. & Wu, C. F. Effects of hyperkinetic, a β subunit of Shaker voltage-dependent K+ channels, on the oxidation state of presynaptic nerve terminals. J. Neurogenet. 22, 103–115 (2008)

  21. 21

    Auld, V. J., Fetter, R. D., Broadie, K. & Goodman, C. S. Gliotactin, a novel transmembrane protein on peripheral glia, is required to form the blood-nerve barrier in Drosophila . Cell 81, 757–767 (1995)

  22. 22

    Saito, M. & Wu, C. F. Expression of ion channels and mutational effects in giant Drosophila neurons differentiated from cell division-arrested embryonic neuroblasts. J. Neurosci. 11, 2135–2150 (1991)

  23. 23

    Bai, J., Sepp, K. J. & Perrimon, N. Culture of Drosophila primary cells dissociated from gastrula embryos and their use in RNAi screening. Nature Protocols 4, 1502–1512 (2009)

  24. 24

    Grueber, W. B. et al. Projections of Drosophila multidendritic neurons in the central nervous system: links with peripheral dendrite morphology. Development 134, 55–64 (2007)

  25. 25

    Grueber, W. B., Jan, L. Y. & Jan, Y. N. Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development 129, 2867–2878 (2002)

  26. 26

    Grueber, W. B., Ye, B., Moore, A. W., Jan, L. Y. & Jan, Y. N. Dendrites of distinct classes of Drosophila sensory neurons show different capacities for homotypic repulsion. Curr. Biol. 13, 618–626 (2003)

  27. 27

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

  28. 28

    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)

  29. 29

    Montell, C. Visual transduction in Drosophila . Annu. Rev. Cell Dev. Biol. 15, 231–268 (1999)

  30. 30

    Thorne, N. & Amrein, H. Atypical expression of Drosophila gustatory receptor genes in sensory and central neurons. J. Comp. Neurol. 506, 548–568 (2008)

  31. 31

    Montell, C., Jones, K., Hafen, E. & Rubin, G. Rescue of the Drosophila phototransduction mutation trp by germline transformation. Science 230, 1040–1043 (1985)

  32. 32

    Rosenzweig, M. et al. The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. Genes Dev. 19, 419–424 (2005)

  33. 33

    Hamada, F. N. et al. An internal thermal sensor controlling temperature preference in Drosophila . Nature 454, 217–220 (2008)

  34. 34

    Kwon, Y., Shim, H. S., Wang, X. & Montell, C. Control of thermotactic behavior via coupling of a TRP channel to a phospholipase C signaling cascade. Nature Neurosci. 11, 871–873 (2008)

  35. 35

    Kang, K. et al. Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception. Nature 464, 597–600 (2010)

  36. 36

    Lee, T. & Luo, L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451–461 (1999)

  37. 37

    White, K. et al. Genetic control of programmed cell death in Drosophila . Science 264, 677–683 (1994)

  38. 38

    Adams, C. M. et al. Ripped pocket and pickpocket, novel Drosophila DEG/ENaC subunits expressed in early development and in mechanosensory neurons. J. Cell Biol. 140, 143–152 (1998)

  39. 39

    Ainsley, J. A., Kim, M. J., Wegman, L. J., Pettus, J. M. & Johnson, W. A. Sensory mechanisms controlling the timing of larval developmental and behavioral transitions require the Drosophila DEG/ENaC subunit, Pickpocket1. Dev. Biol. 322, 46–55 (2008)

  40. 40

    Ainsley, J. A. et al. Enhanced locomotion caused by loss of the Drosophila DEG/ENaC protein Pickpocket1. Curr. Biol. 13, 1557–1563 (2003)

  41. 41

    Xu, K. et al. The fragile X-related gene affects the crawling behavior of Drosophila larvae by regulating the mRNA level of the DEG/ENaC protein Pickpocket1. Curr. Biol. 14, 1025–1034 (2004)

  42. 42

    Kernan, M., Cowan, D. & Zuker, C. Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila . Neuron 12, 1195–1206 (1994)

  43. 43

    Nagel, G. et al. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl Acad. Sci. USA 100, 13940–13945 (2003)

  44. 44

    Schroll, C. et al. Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr. Biol. 16, 1741–1747 (2006)

  45. 45

    Zhang, F., Aravanis, A. M., Adamantidis, A., de Lecea, L. & Deisseroth, K. Circuit-breakers: optical technologies for probing neural signals and systems. Nature Rev. Neurosci. 8, 577–581 (2007)

  46. 46

    Zhong, L., Hwang, R. Y. & Tracey, W. D. Pickpocket is a DEG/ENaC protein required for mechanical nociception in Drosophila larvae. Curr. Biol. 20, 429–434 (2010)

  47. 47

    Pollock, J. A. & Benzer, S. Transcript localization of four opsin genes in the three visual organs of Drosophila; RH2 is ocellus specific. Nature 333, 779–782 (1988)

  48. 48

    Tracey, W. D., Jr, Wilson, R. I., Laurent, G. & Benzer, S. painless, a Drosophila gene essential for nociception. Cell 113, 261–273 (2003)

  49. 49

    Hwang, R. Y. et al. Nociceptive neurons protect Drosophila larvae from parasitoid wasps. Curr. Biol. 17, 2105–2116 (2007)

Download references

Acknowledgements

We thank P. Garrity, C. Desplan, J. Blau, C. Montell, J. Hall, H. Amrein, L. Tian, S. Younger and S. Zhu for fly stocks and reagents; T. Jin for technical support; C. Han for generating whole larval images; H. H. Lee for collaboration to identify the 19-12-GAL4 and 21-7-GAL4 lines; R. Yang, H. H. Lee, B. Ye, J. Parrish, P. Soba, B. Schroeder and J. Bagley for discussions and advice; B. Ye, R. Yang, W. Ge and J. Berg for critical reading of the manuscript; and Jan laboratory members for discussions. Y.X. was a recipient of a Long-term Fellowship from the Human Frontier Science Program, N.V. is supported by Deutsche Forschungsgemeinschaft. This work is supported by a NIH grant (2R37NS040929) to Y.N.J. Y.X. and Q.Y. are associates, L.Y.J. and Y.N.J. are investigators of the Howard Hughes Medical Institute. L.L.L. is supported by the Howard Hughes Medical Institute, Janelia Farm Campus.

Author information

Y.X. designed and carried out the experiments and analysed the data; Q.Y. characterized molecular information of Gr28b, rhodopsin and cryptochrome. L.L.L. created GCaMP3 and did the bioinformatic analyses of Gr28b; N.V. cleaned up the Rh31 and Rh41 mutants; Y.N.J. helped to design the experiments and supervised the work; Y.X., L.L.L., L.Y.J. and Y.N.J. wrote the manuscript.

Correspondence to Yuh Nung Jan.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Figures

The file contains Supplementary Figures 1-26 with legends. (PDF 4377 kb)

Supplementary Movie 1

This movie shows photoavoidance of a wt larva to the light spot of 0.57 mW/mm2. (MOV 5834 kb)

Supplementary Movie 2

This movie shows the photoavoidance of a Bolwig organ-ablated larva (GMR-Hid) to the light spot of 0.57 mW/mm2. (MOV 4546 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Xiang, Y., Yuan, Q., Vogt, N. et al. Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature 468, 921–926 (2010) doi:10.1038/nature09576

Download citation

Further reading

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.