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A gustatory receptor paralogue controls rapid warmth avoidance in Drosophila

Nature volume 500, pages 580–584 (2013)Cite this article

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Abstract

Behavioural responses to temperature are critical for survival, and animals from insects to humans show strong preferences for specific temperatures1,2. Preferred temperature selection promotes avoidance of adverse thermal environments in the short term and maintenance of optimal body temperatures over the long term1,2, but its molecular and cellular basis is largely unknown. Recent studies have generated conflicting views of thermal preference in Drosophila, attributing importance to either internal3 or peripheral4 warmth sensors. Here we reconcile these views by showing that thermal preference is not a singular response, but involves multiple systems relevant in different contexts. We found previously that the transient receptor potential channel TRPA1 acts internally to control the slowly developing preference response of flies exposed to a shallow thermal gradient3. We now find that the rapid response of flies exposed to a steep warmth gradient does not require TRPA1; rather, the gustatory receptor GR28B(D) drives this behaviour through peripheral thermosensors. Gustatory receptors are a large gene family, widely studied in insect gustation and olfaction, and are implicated in host-seeking by insect disease vectors5,6,7, but have not previously been implicated in thermosensation. At the molecular level, GR28B(D) misexpression confers thermosensitivity upon diverse cell types, suggesting that it is a warmth sensor. These data reveal a new type of thermosensory molecule and uncover a functional distinction between peripheral and internal warmth sensors in this tiny ectotherm reminiscent of thermoregulatory systems in larger, endothermic animals2. The use of multiple, distinct molecules to respond to a given temperature, as observed here, may facilitate independent tuning of an animal’s distinct thermosensory responses.

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Figure 1: Gr28b is required for rapid negative thermotaxis.
Figure 2: GR28B(D) expression confers warmth-responsive neuronal activation and behaviour.
Figure 3: GR28B(D) expression yields highly thermosensitive currents.
Figure 4: GR28B(D) and TRPA1(B) functionally substitute for one another.

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  • 19 August 2013

    The sentence starting: ‘To quantify the thermosensitivity...’ was corrected in the HTML.

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Acknowledgements

We thank the Garrity laboratory, C. B. Chien, L. Huang, R. Huey, E. Marder and G. Turrigiano for comments, H. Amrein, Y. Jan, C. Montell, C. Zuker and Bloomington Stock Center for strains, N. Donelson, M. Klein, A. Samuel, T. Lauer, P. Taneja, S. Nelson, Y. Yu, H. Bell, P. Sengupta, F. Baier and L. Vosshall for assistance. Supported by grants from National Institute of Mental Health (NIMH) (EUREKA R01 MH094721), National Institute of Neurological Disorders and Stroke (NINDS) (PO1 NS044232) and National Science Foundation (IOS-1025307) to P.A.G., National Institute of General Medical Sciences (NIGMS) (R01 GM054408) and NIMH (R01 MH067284) to L.C.G., NIGMS (R01 GM094468) to D.L.T. and NINDS National Research Service Award to V.C.P.

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Authors and Affiliations

  1. National Center for Behavioral Genomics, Brandeis University, Waltham, 02454, Massachusetts, USA

    Lina Ni, Peter Bronk, Elaine C. Chang, April M. Lowell, Juliette O. Flam, Vincent C. Panzano, Leslie C. Griffith & Paul A. Garrity

  2. Department of Biology, Volen Center for Complex Systems, Brandeis University, Waltham, 02454, Massachusetts, USA

    Lina Ni, Peter Bronk, Elaine C. Chang, April M. Lowell, Juliette O. Flam, Vincent C. Panzano, Leslie C. Griffith & Paul A. Garrity

  3. Department of Biochemistry, Brandeis University, Waltham, 02454, Massachusetts, USA

    Douglas L. Theobald

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Contributions

L.N., P.B., A.M.L., L.C.G. and P.A.G. designed experiments. L.N. performed molecular genetics, behaviour and chemosensor electrophysiology. P.B. performed neuromuscular electrophysiology. E.C.C., A.M.L. and J.O.F. performed behaviour electrophysiology. V.C.P. performed chemosensor electrophysiology. D.L.T. and P.A.G. performed bioinformatics. L.N., P.B., D.L.T., L.C.G. and P.A.G. wrote the paper.

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Correspondence to Paul A. Garrity.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Figures

This file contains Supplementary Figures 1-9. (PDF 10684 kb)

Warmth-triggered incapacitation of Actin>Gr28b(D) flies

Flies that express Gr28b(D) broadly (Actin-Gal4;UAS-Gr28b(D)) were temporarily incapacitated by warming, while control flies (containing only the Actin-Gal4 source or the UAS-Gr28b(D) transgene) were not. All flies were heated by submerging their vials in a 37˚C water bath for 180 seconds. Some frames were deleted as indicated. The video is accelerated 8-fold. (MOV 6085 kb)

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Ni, L., Bronk, P., Chang, E. et al. A gustatory receptor paralogue controls rapid warmth avoidance in Drosophila. Nature 500, 580–584 (2013). https://doi.org/10.1038/nature12390

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