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Acid sensing by the Drosophila olfactory system

Nature volume 468, pages 691–695 (2010)Cite this article

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Abstract

The odour of acids has a distinct quality that is perceived as sharp, pungent and often irritating1. How acidity is sensed and translated into an appropriate behavioural response is poorly understood. Here we describe a functionally segregated population of olfactory sensory neurons in the fruitfly, Drosophila melanogaster, that are highly selective for acidity. These olfactory sensory neurons express IR64a, a member of the recently identified ionotropic receptor (IR) family of putative olfactory receptors2. In vivo calcium imaging showed that IR64a+ neurons projecting to the DC4 glomerulus in the antennal lobe are specifically activated by acids. Flies in which the function of IR64a+ neurons or the IR64a gene is disrupted had defects in acid-evoked physiological and behavioural responses, but their responses to non-acidic odorants remained unaffected. Furthermore, artificial stimulation of IR64a+ neurons elicited avoidance responses. Taken together, these results identify cellular and molecular substrates for acid detection in the Drosophila olfactory system and support a labelled-line mode of acidity coding at the periphery.

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Figure 1: Identification of a glomerulus, DC4, activated by the CO 2 metabolite carbonic acid.
Figure 2: DC4 is innervated by coeloconic sensillar neurons expressing IR64a.
Figure 3: Activation of DC4 by acidity requires IR64a.
Figure 4: IR64a+ neurons and IR64a are necessary and sufficient for avoidance behaviour.
Figure 5: Fruit flies are attracted to components other than acetic acid in vinegar.

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Acknowledgements

We thank M. Dus for helpful discussions and technical support for making anti-IR64a antibody; M. Kim for technical assistance; J. Treisman, N. Ringstad, C. Desplan, M. Warman, G. Fishell, M. Chesler, A. Wong, L. Vosshall and D. Anderson for discussions and comments on the manuscript; and R. Lehmann for sharing her two-photon microscope. This work was initiated in D. Anderson’s laboratory at California Institute of Technology. G.S.B.S. thanks H.-R. Song for support. Financial support was provided by a National Research Service Award fellowship (M.A.), the Boehringer Ingelheim Foundation (R. Bell), the Centre National de la Recherche Scientifique (Y.G.), a European Research Council Starting Independent Researcher Grant (R. Benton), the Swiss National Science Foundation (R. Benton), the Alfred P. Sloan Foundation (G.S.), the Whitehall Foundation (G.S.), a Whitehead President Award (G.S.) and NIH grant 1RO1GM089746 (G.S).

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Author notes

  1. Yael Grosjean & Charlotte Leblanc

    Present address: Present addresses: Centre des Sciences du Goût et de l’Alimentation, UMR-6265 CNRS, UMR-1324 INRA, Université de Bourgogne, 6 Boulevard Gabriel, 21000 Dijon, France (Y.G.); Université Paris Diderot – Paris 7, 16 rue Marguerite Duras, 75013 Paris, France (C.L.).,

  2. Minrong Ai and Soohong Min: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Cell Biology, Molecular Neurobiology Program, Skirball Institute of Biomolecular Medicine, New York University, School of Medicine, New York, 10016, New York, USA

    Minrong Ai, Soohong Min, Charlotte Leblanc & Greg S. B. Suh

  2. Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, Lausanne, CH-1015, Switzerland

    Yael Grosjean, Rati Bell & Richard Benton

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Contributions

G.S.B.S. identified the GC16-GAL4 line from a screen and performed initial imaging experiments. M.A. generated most of the transgenic flies, performed calcium imaging and some behavioural experiments, and conducted immunohistochemistry. S.M. performed most of the behavioural testing and immunohistochemistry. C.L. assisted in characterizing IR64a mutant alleles. Y.G., R. Bell and R. Benton generated IR64a-GAL4 and UAS-IR64a transgenic flies and showed that IR64a+ neurons innervate the DC4 and DP1m glomeruli. M.A. and G.S.B.S. analysed and interpreted the data and wrote the manuscript with inputs from all the authors.

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Correspondence to Greg S. B. Suh.

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The authors declare no competing financial interests.

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Ai, M., Min, S., Grosjean, Y. et al. Acid sensing by the Drosophila olfactory system. Nature 468, 691–695 (2010). https://doi.org/10.1038/nature09537

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