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Logo of nihpaAbout Author manuscriptsSubmit a manuscriptNIH Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
Nature. Author manuscript; available in PMC Jan 25, 2011.
Published in final edited form as:
PMCID: PMC3026603
NIHMSID: NIHMS261312

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

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.

Light sensing is critical for animal life. Whereas image-forming visual perception allows animals to identify and track mates, predators and prey, non-image-forming functions regulate pupil reflex, phototaxis and circadian entrainment1,2. In addition to eyes1,2, extra-ocular photoreceptors exist15. For example, many eyeless or blinded animals can sense illumination of their body surfaces35. Birds possess deep-brain photoreceptors in their hypothalamus6, and extra-ocular photoreceptors are required for magnetic orientation of amphibians7. Recent studies demonstrate that eyeless animals such as Caenorhabditis elegans nonetheless have photoreceptors controlling light avoidance810.

Drosophila larvae spend most of the time feeding by digging into food. Light avoidance is a crucial behaviour to minimize body exposure. When tested in groups in a dark/light choice assay, Drosophila larvae prefer darkness11,12. This behaviour requires the pair of Bolwig organs on the larval head12; that is, primitive eye structures each comprised of 12 photoreceptors expressing Rh5 or Rh6, rhodopsins sensing blue and green light, respectively13.

Cells besides Bolwig organs contribute to photoavoidance

We designed a photoavoidance assay for a single larva with sunlight-level intensities (−1 mW mm−2 in San Francisco on a clear day in June, consistent with previous reports14). Wild-type Drosophila larvae showed avoidance of a white light spot of 0.57 mW mm−2 (Fig. 1a and Supplementary Movie 1). Surprisingly, similar avoidance (Fig. 1b and Supplementary Movie 2) was exhibited by larvae with their Bolwig organs ablated by the pro-apoptotic gene Head involution defective (Hid; also called Wrinkled (W))15 expressed via the Bolwig-organ-specific promoter Glass Multimer Reporter (GMR)16 (Supplementary Fig. 1a). Lower light intensities elicited less photoavoidance of wild-type animals, and even less of Bolwig-organ-ablated animals (Fig. 1c). However, at light intensities of 0.57 mW mm−2 or higher, GMR-Hid larvae showed avoidance comparable to wild-type animals (P >0.05). Thus, although the Bolwig organs are responsible for dim light avoidance and dark congregation12, Drosophila larvae must contain extra-ocular photoreceptors.

Figure 1
Photoreceptors in addition to Bolwig organs contribute to photoavoidance

Testing the wavelength dependence of photoavoidance using bandpass filters letting through ultraviolet (−360 nm; Fig. 1d), violet (−402 nm; Fig. 1e), blue (−470 nm; Fig. 1f), green (−525 nm; Fig. 1g) or red light (−620 nm; Fig. 1h), we found that wild-type animals showed increased photoavoidance with higher light intensity (Fig. 1d–h), and were most sensitive to blue, violet and ultraviolet, and largely unresponsive to green and red light. Bolwig-organ-ablated animals showed less photoavoidance at low light intensity, but exhibited nearly normal avoidance response to high-intensity, short-wavelength light (Fig. 1d–f), demonstrating the existence of light-sensitive cells in addition to Bolwig organs. Because there was no detectable temperature increase associated with 0.11 mW mm−2 violet light (Supplementary Fig. 2)—which triggered avoidance in nearly 80% of the wild-type and GMR-Hid animals—and animals showed little response to high-intensity green or red light but strongly avoided low-intensity short-wavelength light (Fig. 1d–h), light avoidance probably involves wavelength-dependent photoreceptors but not local heating.

Class IV neurons tiling larval body wall sense light

Given the report of diffusely distributed dermal photoreceptors triggering shadow reaction35, we tested whether sensory neurons in the larval body wall could be candidate photoreceptors. Using GCaMP3, a genetically encoded calcium indicator1719, we found that blue light delivered for 5 s to the dorsal cluster (Fig. 2a, see Fig. 3c for whole larva image) generated a marked fluorescence increase specifically in the soma, axon and dendrites of ddaC, a class IV dendritic arborization neuron (Fig. 2b, e, f), but not in nearby sensory neurons (Fig. 2b, e, f). ddaC also responded to ultraviolet light (which also caused photo-bleaching), but not to green light (Fig. 2c–f). There were also Ca2+ increases specifically in class IV dendritic arborization neurons of the ventral and lateral cluster (V′ada and VdaB, respectively) in response to ultraviolet and blue light, but not green light (Supplementary Figs 3 and 4). Similar GCaMP3 fluorescence responses were seen in class IV dendritic arborization neurons in body segments from head to tail (Supplementary Fig. 5).

Figure 2
Light activates class IV dendritic arborization neurons
Figure 3
Cell-autonomous activation of class IV dendritic arborization neurons by light

Extracellular recording further revealed a progressive increase in action potential frequency when the dorsal class IV dendritic arborization neuron ddaC was illuminated with increasing intensity of blue light (Fig. 2g), ultraviolet light and violet light, but not red light (Supplementary Fig. 6). Responses were: 340 nm > 380 nm > 402 nm >470 nm [dbl greater-than sign]525 nm or 620 nm light (Fig. 2h).

The wavelength dependence of ddaC firing rate increase was similar to that observed with GCaMP3 imaging and the light avoidance behavioural assay. The latency between the onset of light stimulation and action potential burst firing decreased with higher light intensity, and was as short as 1 s with bright illumination (Supplementary Fig. 6). When illuminated with 1.4 mW mm−2 of white light (approximating sunlight), ddaC neurons in the dorsal cluster showed a significant firing increase (Fig. 2i). Similar robust activation of ventral (VdaB) and lateral (V′ada) class IV dendritic arborization neurons was induced by 52.8 mW mm−2 blue light (Supplementary Fig. 7a, b). The response of class IV dendritic arborization neurons was similar regardless of their location along the body axis (data not shown), as in the case of GCaMP3 imaging (Supplementary Fig. 5).

We did not observe any significant effects of light on firing rate of class I or III dendritic arborization neurons (Supplementary Fig. 7c, d, P >0.05). Because class I dendritic arborization neurons progressively increased their firing rate as the temperature was raised above 30 °C, whereas class IV dendritic arborization neurons showed an abrupt increase of firing rate only above 40 °C (Supplementary Fig. 8), thermal responses cannot account for the light-induced increase of firing in class IV but not class I dendritic arborization neurons. Moreover, application of 10 μM H2O2, which elevates the reactive oxygen species (ROS) level in Drosophila larvae20, had no effect on the firing rate of class IV dendritic arborization neurons (Supplementary Fig. 9). These studies demonstrate that ultraviolet, violet and blue light activate class IV dendritic arborization neurons in an intensity-dependent manner. Responses occur at sunlight-level intensities, are not induced by heat or ROS, correlate with behaviour, and are confined to this specific class of sensory neurons throughout the animal.

Light activates class IV neurons and dendrites in isolation

The dendritic arborization neurons have dendrites in contact with epithelial cells whereas their somas and axons are wrapped by glia21. To test whether class IV dendritic arborization neurons can sense light by themselves, we prepared primary neuronal cultures22,23 from embryos expressing GCaMP3 and RFP specifically in class IV dendritic arborization neurons by means of pickpocket-GAL4 (ppk-GAL4)24. Ultraviolet and blue light illumination of isolated class IV dendritic arborization neurons generated a robust increase of GCaMP3 signals (Fig. 3a and Supplementary Fig. 10). In contrast, cultured class III dendritic arborization neurons expressing GCaMP3 and RFP via 19-12-GAL4 yielded no light response (Fig. 3b). Thus, class IV dendritic arborization neurons have the intrinsic ability to detect light.

Dendrites of class IV dendritic arborization neurons tile the larval body wall with non-overlapping but complete coverage of the dendritic field25,26 (Fig. 3c). Illumination of only the dendrites of class IV dendritic arborization neurons (Fig. 3d) with ultraviolet, violet and blue light, but not green or red light, activated the neurons (Fig. 3e). The activation spectrum is similar to that for illumination of the entire class IV dendritic arborization neurons (Fig. 2h), indicating the presence of phototransduction machinery in the dendrites.

Gr28b is critical for light transduction in class IV neurons

No defects in light response of class IV dendritic arborization neurons were found in available mutants of rhodopsins13,27 and cryptochrome (cry)28, as well as a mutant in no receptor potential A (norpA), which encodes phospholipase C (PLC), downstream of rhodopsins29 (Fig. 4a). We then tested the Drosophila homologue of Lite-1, a C. elegans light sensor810. The closest homologue of lite-1 in Drosophila is gustatory receptor 28b (Gr28b), annotated as encoding a gustatory G-protein-coupled receptor. Several Gr28b-GAL4 lines carrying different promoter regions revealed consistent expression in all class IV dendritic arborization neurons, two sensory neurons in the lateral body wall, plus several neurons in the ventral nerve cord (Supplementary Fig. 11), as reported previously30. To test for the functional role of Gr28b in the light-induced electrophysiological responses, we recorded from class IV dendritic arborization neurons in Dmel\Mi{ET1}Gr28bMB03888 (MiET1) and Dmel\PBac{PB}Gr28bc01884 (PBac) larvae with P-element insertion into the Gr28b coding and intronic regions, respectively (http://flybase.org/reports/FBgn0045495.html). Whereas these P-element insertions did not alter the basal firing rate (data not shown), they caused a significant reduction in light-induced responses of class IV dendritic arborization neurons (Fig. 4b), as in hemizygous larvae carrying one MiET1 allele and one deletion encompassing Gr28b (Df(2L)Exel7031; http://flybase.org/reports/FBab0037910.html) (Fig. 4c). The MiET1 P-element inserts into the coding sequence common to all reported transcripts, and its mobilization for excision restored the light-induced response in class IV dendritic arborization neurons (Fig. 4d). Moreover, knockdown of Gr28b expression with UAS-RNAi driven by ppk-GAL4 caused an overall reduction of light response of class IV dendritic arborization neurons (Fig. 4e). Taken together, our data indicate that Gr28b is expressed in class IV dendritic arborization neurons, and is required for proper light responses. Whether Gr28b is the direct photosensing molecule awaits further experimentation.

Figure 4
Gr28b and TrpA1 are essential for class IV dendritic arborization neuron light responses

Sequence analysis revealed that Gr28b has a rhodopsin-like structure plus one extra transmembrane segment (Supplementary Fig. 12), raising the question of whether the Gr28b-dependent light response involves G-protein signalling. To test whether G-protein signalling is required in class IV dendritic arborization neurons, we applied the myristoylated βγ-binding peptide mSIRK, and found that the light response in class IV dendritic arborization neurons was significantly reduced (Supplementary Fig. 13). Thus, G-protein signalling is probably involved in the light response of class IV dendritic arborization neurons, similar to findings in C. elegans10. We further tested cyclic nucleotide-gated (CNG) channels, which are known to act downstream of Lite-1 and G proteins in C. elegans10. Unlike in C. elegans, blocking CNG channels with L-cis-diltiazem in class IV dendritic arborization neurons had no effect on their light responses (Supplementary Fig. 14).

TrpA1 is required in light transduction in class IV neurons

Transient receptor potential (TRP) channels were first identified and characterized in the Drosophila compound eye29,31, with TRP and TRP-like (trpl) having key roles in phototransduction29. However, our electrophysiological studies revealed no defects in the light response of class IV dendritic arborization neurons in trpl or painless mutant larvae (Supplementary Fig. 15).

TrpA1, a Drosophila homologue of mammalian TrpA, may function as a thermosensor in larvae and adults3234, and a receptor for reactive electrophiles such as allyl isothiocyanate (AITC)35. A TrpA1 mutant exhibited normal basal firing in class IV dendritic arborization neurons (data not shown), but no light-induced firing increase (Fig. 4f). As reported previously32, we detected strong TrpA1 immunoreactivity in several neurons in the larval brain but not in peripheral neurons (data not shown). We then performed MARCM (mosaic analysis with a repressible cell marker)36, and found no light response in class IV dendritic arborization neurons lacking TrpA1 (Fig. 4g), and a significant reduction of light-induced firing of the heterozygous class IV dendritic arborization neurons (Supplementary Fig. 16), indicating that TrpA1 is present in levels below immunodetection, but nonetheless of functional importance. In support of this notion, AITC caused strong activation of class IV dendritic arborization neurons, and this activation was abolished in the TrpA1 mutant (Supplementary Fig. 17a). Moreover, TrpA1 RNAi expression specifically in class IV dendritic arborization neurons eliminated the light-induced firing change (Supplementary Fig. 18). Taken together, our observations suggest that TrpA1 is required cell-autonomously for light transduction in class IV dendritic arborization neurons.

Given the lack of AITC activation of class I or class III dendritic arborization neurons (Supplementary Fig. 17b), we expressed TrpA1 in class I dendritic arborization neurons and found that it conferred AITC sensitivity but not light response (Supplementary Fig. 17c, d), indicating that TrpA1 is not sufficient for light sensing. Because trans-heterozygotes carrying one mutant allele of TrpA1 and one copy of the MiET1 P-element insertion in the Gr28b gene showed reduced light response (Supplementary Fig. 19), it is likely that Gr28b and TrpA1 function in the same phototransduction pathway.

Class IV neurons mediate light avoidance behaviour

To test whether class IV dendritic arborization neurons are involved in light avoidance, we genetically ablated class IV dendritic arborization neurons of third instar larvae by expressing the pro-apoptotic genes Hid (ref. 15) and reaper (rpr) (ref. 37) via ppk-GAL4 (ppk-GAL4; UAS-Hid, rpr) (Supplementary Fig. 1). We also constructed a line lacking Bolwig organs as well as class IV dendritic arborization neurons (UAS-Hid, rpr; GMR-Hid; ppk-GAL4). Notably, both lines showed markedly decreased white-light-avoidance behaviour compared to wild-type and GMR-Hid (Bolwig-organ-ablated) larvae (Fig. 5a, b). Class IV dendritic-arborization-neurons-ablated animals showed a significant decrease of avoidance versus wild type, for all white light intensities tested (Fig. 5c–g). Ablation of class IV dendritic arborization neurons in animals lacking Bolwig organs produced a further decrease in white light avoidance (Fig. 5d–g). Avoidance of high-intensity (>0.57 mW mm−2) white light was normal when Bolwig organs were ablated in wild type (Fig. 5e–g), and in control strains with either GAL4 or UAS (Fig. 5f). Taken together with similar findings with ultraviolet, violet and blue light (Supplementary Figs 20–22), these results demonstrate that class IV dendritic arborization neurons are necessary to elicit photoavoidance at high intensities. It thus seems that the Bolwig organs and class IV dendritic arborization neurons operate in different light intensity regimes: Bolwig organs are tuned to low light, whereas class IV dendritic arborization neurons, required in low light, are the primary sensors at high intensities.

Figure 5
Class IV dendritic arborization neurons are the extra-ocular photoreceptors that contribute to light avoidance

Careful examination of ppk-GAL4 revealed additional expression in four mouth hook neurons, but not in the central nervous system (Supplementary Fig. 23a–d). Laser ablation of these four neurons in the GMR-Hid background had no effect on light avoidance behaviour (Supplementary Fig. 23e). Therefore, the class IV dendritic arborization neurons in the body wall are the ones important for the light avoidance behaviour.

Pickpocket, a Degenerin/Epithelial sodium Channel (DEG/ENaC) family member specifically expressed in class IV dendritic arborization neurons24,38 (Fig. 3c), has been implicated in locomotion control3941. However, nose-touch experiments42 revealed that larvae lacking class IV dendritic arborization neurons responded normally to gentle touch by retracting or turning away their heads (Supplementary Fig. 24). Moreover, direct recording of class IV dendritic arborization neurons in ppk mutant larvae revealed no defect in light response (Supplementary Fig. 15b). These results demonstrate that reduced light avoidance in class IV dendritic-arborization-ablated larvae is not due to non-specific effects.

To probe sufficiency, we expressed channelrhodopsin-2 (ChR2), a retinal-dependent cation channel gated by light from ultraviolet to green4345, specifically in class IV dendritic arborization neurons. ChR2 conferred green light sensitivity to dendritic arborization neurons from larvae fed with retinal (Supplementary Fig. 25), as well as robust avoidance of green light of retinal-fed larvae without Bolwig organs (Fig. 5h). Thus, activation of class IV dendritic arborization neurons is sufficient to induce avoidance.

With or without Bolwig organs, TrpA1 mutant larvae showed deficient avoidance of 1 mW mm−2 white light (Fig. 5i). Moreover, reducing TrpA1 expression in class IV dendritic arborization neurons by RNAi was sufficient to abolish the light avoidance behaviour in animals without Bolwig organs (Supplementary Fig. 26). Together, our physiological and behavioural studies indicate that a light transduction pathway involving TrpA1 and Gr28b in class IV dendritic arborization neurons is necessary for light avoidance.

Discussion

Extra-ocular photoreceptors, previously found in reptiles, birds, amphibians and fish, provide a good measure of ambient light luminance and serve mainly non-image-forming functions such as phototaxis, circadian photo-entrainment, pupal reflex, shadow reaction and magnetic orientation17. Usually, these extra-ocular photoreceptors have much lower light sensitivity and slower kinetics than ocular photoreceptors3.

Drosophila larvae have primitive eye structures, the Bolwig organs, which control avoidance of dim light12. Here we report that the class IV dendritic arborization neurons, previously implicated in mechanosensory response and motion control3841,46, are surprisingly also photoreceptors. Our behavioural analysis suggests that Bolwig organs and class IV dendritic arborization neurons have different regimes of light sensing in acute photoavoidance. Bolwig organs, packed with photopigments47, are preferentially required for avoidance of low light. Class IV dendritic arborization neurons, which also contribute to low light avoidance, are the primary sensors at sunlight-level intensities. This organization ensures that larvae can detect the full range of ambient light intensities, from dim to strong.

Class IV dendritic arborization neurons have the intrinsic ability to sense light, even after isolation in culture, and their dendrites are capable of sensing light (Fig. 3 and Supplementary Fig. 10). Importantly, the dendrites of class IV dendritic arborization neurons have complete and non-redundant coverage of the body wall (Fig. 3c), allowing animals to perceive illumination of any body part, and initiate an appropriate behavioural response. Larvae spend much of the time with their heads digging into food, making their Bolwig organs on the head less likely to be exposed to light. Thus, the ability to sense light with sensory neurons tiling the body wall is critical for detection of exposure.

Class IV dendritic arborization neurons use a novel light transduction pathway. Like in C. elegans, a putative chemosensory G-protein-coupled receptor, Gr28b, is involved for phototransduction in class IV dendritic arborization neurons (Fig. 4b–e). TrpA1 also is essential (Fig. 4f, g and Supplementary Fig. 18). Drosophila larval class IV dendritic arborization neurons may function as nociceptors46,48,49. They are required for thermal and mechanical nociception, and activation of class IV dendritic arborization neurons is sufficient to induce a behaviour pattern similar to nocifension46,48,49. Given that class IV dendritic arborization neurons are required for larvae to avoid harmful light stimuli, these neurons seem to be poised to alert the animal to a variety of adversities.

Our study has uncovered unexpected light-sensing machinery, which could be critical for foraging larvae to avoid harmful sunlight, desiccation and predation. By providing precedence for photoreceptors strategically placed away from the eyes, our finding of an array of class IV dendritic arborization neurons with elaborate dendrites tiling the entire body wall, and acting as light-sensing antennae, raises the question of whether other animals with eyes might also possess extra-ocular photoreceptors for more thorough light detection and behavioural response.

METHODS SUMMARY

Light avoidance assay

Light avoidance was scored if the third instar larva reversed in direction or turned its head completely away from the 1.7-mm light spot on its head during the 5-s illumination. Two-tailed Fisher exact test (20–40 larvae per condition), *P <0.05, **P <0.01, ***P <0.001.

Electrophysiology

Action potentials were monitored via extracellular recordings from a third instar larval fillet with muscles removed, using an Axon 700B amplifier and pCLAMP 10 software.

GCaMP3 imaging

Third instar larval fillets were imaged on a Zeiss LS510 META confocal microscope with an Olympus ×40/0.8 NA water immersion objective, with a 488-nm laser. GCaMP3 cDNA is available from AddGene.

Cell culture

Embryos homozygous for Canton S (Cs); UAS-GCaMP3; ppk-GAL4, UAS-RFP (for class IV dendritic arborization neuron culture) or Cs; UAS-GCaMP3; 19-12-GAL4, UAS-RFP (for class III dendritic arborization neuron culture) were used for culture22,23.

MARCM analysis

We recorded from class IV dendritic arborization neuron clones marked with GFP for lacking TrpA1 (ref. 36).

Full Methods and any associated references are available in the online version of the paper at www.nature.com/nature.

Supplementary Material

Fig 1-26

Acknowledgments

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.

Footnotes

Supplementary Information is linked to the online version of the paper at www.nature.com/nature.

Author 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.

Author Information Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests. Readers are welcome to comment on the online version of this article at www.nature.com/nature.

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