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

Nature volume 468, pages 921–926 (2010)Cite this article

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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.

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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.

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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.

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Authors and Affiliations

  1. Departments of Physiology, Howard Hughes Medical Institute, Biochemistry, and Biophysics, University of California San Francisco, San Francisco, 94158, California, USA

    Yang Xiang, Quan Yuan, Lily Yeh Jan & Yuh Nung Jan

  2. Center for Developmental Genetics, New York University, New York, 10003, New York, USA

    Nina Vogt

  3. Howard Hughes Medical Institute, Janelia Farm Research Campus, Ashburn, 20147, Virginia, USA

    Loren L. Looger

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Contributions

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.

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Correspondence to Yuh Nung Jan.

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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)

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

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