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An olfactory receptor for food-derived odours promotes male courtship in Drosophila

Nature volume 478, pages 236–240 (2011)Cite this article

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Abstract

Many animals attract mating partners through the release of volatile sex pheromones, which can convey information on the species, gender and receptivity of the sender to induce innate courtship and mating behaviours by the receiver1. Male Drosophila melanogaster fruitflies display stereotyped reproductive behaviours towards females, and these behaviours are controlled by the neural circuitry expressing male-specific isoforms of the transcription factor Fruitless (FRUM)2,3,4,5. However, the volatile pheromone ligands, receptors and olfactory sensory neurons (OSNs) that promote male courtship have not been identified in this important model organism. Here we describe a novel courtship function of Ionotropic receptor 84a (IR84a), which is a member of the chemosensory ionotropic glutamate receptor family6, in a previously uncharacterized population of FRUM-positive OSNs. IR84a-expressing neurons are activated not by fly-derived chemicals but by the aromatic odours phenylacetic acid and phenylacetaldehyde, which are widely found in fruit and other plant tissues7 that serve as food sources and oviposition sites for drosophilid flies8. Mutation of Ir84a abolishes both odour-evoked and spontaneous electrophysiological activity in these neurons and markedly reduces male courtship behaviour. Conversely, male courtship is increased—in an IR84a-dependent manner—in the presence of phenylacetic acid but not in the presence of another fruit odour that does not activate IR84a. Interneurons downstream of IR84a-expressing OSNs innervate a pheromone-processing centre in the brain. Whereas IR84a orthologues and phenylacetic-acid-responsive neurons are present in diverse drosophilid species, IR84a is absent from insects that rely on long-range sex pheromones. Our results suggest a model in which IR84a couples food presence to the activation of the fruM courtship circuitry in fruitflies. These findings reveal an unusual but effective evolutionary solution to coordinate feeding and oviposition site selection with reproductive behaviours through a specific sensory pathway.

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Figure 1: Gene targeting of Ir84a , a candidate olfactory receptor in the fru M circuit.
Figure 2: Essential requirement for IR84a for spontaneous and odour-evoked neuronal responses.
Figure 3: IR84a is required for male courtship behaviour.
Figure 4: Anatomical integration of VL2a (IR84a-expressing) projection neurons in the pheromone processing centre.

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References

  1. Wyatt, T. D. Pheromones and Animal Behaviour: Communication by Smell and Taste (Oxford Univ. Press, 2003)

    Book  Google Scholar 

  2. Dickson, B. J. Wired for sex: the neurobiology of Drosophila mating decisions. Science 322, 904–909 (2008)

    Article  ADS  CAS  Google Scholar 

  3. Demir, E. & Dickson, B. J. fruitless splicing specifies male courtship behavior in Drosophila . Cell 121, 785–794 (2005)

    Article  CAS  Google Scholar 

  4. Manoli, D. S. et al. Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 436, 395–400 (2005)

    Article  ADS  CAS  Google Scholar 

  5. Stockinger, P., Kvitsiani, D., Rotkopf, S., Tirian, L. & Dickson, B. J. Neural circuitry that governs Drosophila male courtship behavior. Cell 121, 795–807 (2005)

    Article  CAS  Google Scholar 

  6. Benton, R., Vannice, K. S., Gomez-Diaz, C. & Vosshall, L. B. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila . Cell 136, 149–162 (2009)

    Article  CAS  Google Scholar 

  7. Wightman, F. & Lighty, D. L. Identification of phenylacetic acid as a natural auxin in the shoots of higher plants. Physiol. Plant. 55, 17–24 (1982)

    Article  CAS  Google Scholar 

  8. Markow, T. A. & O’Grady, P. Reproductive ecology of Drosophila . Funct. Ecol. 22, 747–759 (2008)

    Article  Google Scholar 

  9. Silbering, A. F. et al. Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems. J. Neurosci. 10.1523/JNEUROSCI.2360-11.2011 (21 September 2011)

  10. Abuin, L. et al. Functional architecture of olfactory ionotropic glutamate receptors. Neuron 69, 44–60 (2011)

    Article  CAS  Google Scholar 

  11. van der Goes van Naters, W. & Carlson, J. R. Receptors and neurons for fly odors in Drosophila . Curr. Biol. 17, 606–612 (2007)

    Article  CAS  Google Scholar 

  12. Ferveur, J. F. Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav. Genet. 35, 279–295 (2005)

    Article  Google Scholar 

  13. Yao, C. A., Ignell, R. & Carlson, J. R. Chemosensory coding by neurons in the coeloconic sensilla of the Drosophila antenna. J. Neurosci. 25, 8359–8367 (2005)

    Article  CAS  Google Scholar 

  14. Barata, A. et al. Analytical and sensorial characterization of the aroma of wines produced with sour rotten grapes using GC-O and GC-MS: identification of key aroma compounds. J. Agric. Food Chem. 59, 2543–2553 (2011)

    Article  CAS  Google Scholar 

  15. Kim, J., Jeon, C. O. & Park, W. A green fluorescent protein-based whole-cell bioreporter for the detection of phenylacetic acid. J. Microbiol. Biotechnol. 17, 1727–1732 (2007)

    CAS  PubMed  Google Scholar 

  16. Bray, S. & Amrein, H. A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship. Neuron 39, 1019–1029 (2003)

    Article  CAS  Google Scholar 

  17. Kohatsu, S., Koganezawa, M. & Yamamoto, D. Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila . Neuron 69, 498–508 (2011)

    Article  CAS  Google Scholar 

  18. Kurtovic, A., Widmer, A. & Dickson, B. J. A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446, 542–546 (2007)

    Article  ADS  CAS  Google Scholar 

  19. Root, C. M. et al. A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59, 311–321 (2008)

    Article  CAS  Google Scholar 

  20. Wang, L. et al. Hierarchical chemosensory regulation of male–male social interactions in Drosophila . Nature Neurosci. 14, 757–762 (2011)

    Article  CAS  Google Scholar 

  21. Vosshall, L. B. & Stocker, R. F. Molecular architecture of smell and taste in Drosophila . Annu. Rev. Neurosci. 30, 505–533 (2007)

    Article  CAS  Google Scholar 

  22. Jefferis, G. S. et al. Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128, 1187–1203 (2007)

    Article  CAS  Google Scholar 

  23. Cachero, S., Ostrovsky, A. D., Yu, J. Y., Dickson, B. J. & Jefferis, G. S. Sexual dimorphism in the fly brain. Curr. Biol. 20, 1589–1601 (2010)

    Article  CAS  Google Scholar 

  24. Yu, J. Y., Kanai, M. I., Demir, E., Jefferis, G. S. & Dickson, B. J. Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr. Biol. 20, 1602–1614 (2010)

    Article  CAS  Google Scholar 

  25. Croset, V. et al. Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet. 6, e1001064 (2010)

    Article  Google Scholar 

  26. Ewing, A. W. & Manning, A. The effect of exogenous scent on the mating of Drosophila melanogaster . Anim. Behav. 11, 596–598 (1963)

    Article  Google Scholar 

  27. Shorey, H. H. & Bartell, R. J. Role of a volatile female sex pheromone in stimulating male courtship behaviour in Drosophila melanogaster . Anim. Behav. 18, 159–164 (1970)

    Article  CAS  Google Scholar 

  28. Spieth, H. T. Courtship behavior in Drosophila . Annu. Rev. Entomol. 19, 385–405 (1974)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  30. Lai, S. L. & Lee, T. Genetic mosaic with dual binary transcriptional systems in Drosophila . Nature Neurosci. 9, 703–709 (2006)

    Article  CAS  Google Scholar 

  31. Han, D. D., Stein, D. & Stevens, L. M. Investigating the function of follicular subpopulations during Drosophila oogenesis through hormone-dependent enhancer-targeted cell ablation. Development 127, 573–583 (2000)

    CAS  PubMed  Google Scholar 

  32. Rong, Y. S. et al. Targeted mutagenesis by homologous recombination in D. melanogaster . Genes Dev. 16, 1568–1581 (2002)

    Article  CAS  Google Scholar 

  33. Bischof, J., Maeda, R. K., Hediger, M., Karch, F. & Basler, K. An optimized transgenesis system for Drosophila using germ-line-specific φC31 integrases. Proc. Natl Acad. Sci. USA 104, 3312–3317 (2007)

    Article  ADS  CAS  Google Scholar 

  34. Benton, R., Sachse, S., Michnick, S. W. & Vosshall, L. B. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo . PLoS Biol. 4, e20 (2006)

    Article  Google Scholar 

  35. Alcorta, E. & Rubio, J. Intrapopulational variation of olfactory responses in Drosophila melanogaster . Behav. Genet. 19, 285–299 (1989)

    Article  CAS  Google Scholar 

  36. Wong, A. M., Wang, J. W. & Axel, R. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109, 229–241 (2002)

    Article  CAS  Google Scholar 

  37. Yu, H. H. et al. A complete developmental sequence of a Drosophila neuronal lineage as revealed by twin-spot MARCM. PLoS Biol. 8, e1000461 (2010)

    Article  Google Scholar 

  38. Chiang, A. S. et al. Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution. Curr. Biol. 21, 1–11 (2011)

    Article  CAS  Google Scholar 

  39. Rueckert, D. et al. Nonrigid registration using free-form deformations: application to breast MR images. IEEE Trans. Med. Imaging 18, 712–721 (1999)

    Article  CAS  Google Scholar 

  40. Evers, J. F., Schmitt, S., Sibila, M. & Duch, C. Progress in functional neuroanatomy: precise automatic geometric reconstruction of neuronal morphology from confocal image stacks. J. Neurophysiol. 93, 2331–2342 (2005)

    Article  CAS  Google Scholar 

  41. Barber, C. B., Dobkin, D. P. & Huhdanpaa, H. The Quickhull algorithm for convex hulls. ACM Trans. Math. Softw. 22, 469–483 (1996)

    Article  MathSciNet  Google Scholar 

  42. Guindon, S. & Gascuel, O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696–704 (2003)

    Article  Google Scholar 

  43. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004)

    Article  CAS  Google Scholar 

  44. Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127–128 (2007)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to B. Dickson, A. Hofbauer, T. Lee, the Bloomington Drosophila Stock Center, the Drosophila Species Stock Center and the Developmental Studies Hybridoma Bank for provision of plasmid vectors, Drosophila strains and antibodies. We are also grateful to A. Wong, J. Wang, R. Axel, H.-H. Yu and T. Lee for sharing raw image data. We thank D. Featherstone, J.-F. Ferveur, T. Kawecki, L. Keller, S. Martin and members of the Benton laboratory for comments on the manuscript. Y.G., J.-P.F. and J.C. are supported by the Centre National de la Recherche Scientifique (CNRS), the Agence Nationale de la Recherche (ANR; JCJC, GGCB-2010) and the Conseil Régional de Bourgogne (FABER). R.R. was supported by a Roche Research Foundation fellowship. G.S.X.E.J. is supported by the Medical Research Council and a European Research Council Starting Investigator Grant. Research in R.B.’s laboratory is supported by the University of Lausanne, a European Research Council Starting Independent Researcher Grant and the Swiss National Science Foundation.

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Authors and Affiliations

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

    Yael Grosjean, Raphael Rytz, Liliane Abuin & Richard Benton

  2. Centre des Sciences du Goût et de l’Alimentation, UMR-6265 CNRS, UMR-1324 INRA, Université de Bourgogne, 6 Boulevard Gabriel, 21000 Dijon, France ,

    Yael Grosjean, Jean-Pierre Farine & Jérôme Cortot

  3. Division of Neurobiology, MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, UK,

    Gregory S. X. E. Jefferis

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Contributions

Y.G. and R.B. conceived the project. Y.G. performed the gene-targeting screen, contributed to the histological analysis and performed most of the behavioural experiments. R.R. performed the electrophysiological odour response screen, the fly odour stimulation assays and the phylogenetic analyses. J.-P.F. performed the chemical analysis. L.A. assisted in the generation and characterization of transgenic flies and contributed to the histological analysis. J.C. contributed to the behavioural experiments. G.S.X.E.J. performed the analysis of projection neurons. R.B. generated the DNA constructs, performed all other electrophysiological analyses and wrote the paper with contributions from Y.G., R.R., J.-P.F. and G.S.X.E.J.

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Correspondence to Richard Benton.

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Grosjean, Y., Rytz, R., Farine, JP. et al. An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature 478, 236–240 (2011). https://doi.org/10.1038/nature10428

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