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A glial amino-acid transporter controls synapse strength and courtship in Drosophila

Nature Neuroscience volume 11, pages 54–61 (2008)Cite this article

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Abstract

Mate choice is an evolutionarily critical decision that requires the detection of multiple sex-specific signals followed by central integration of these signals to direct appropriate behavior. The mechanisms controlling mate choice remain poorly understood. Here, we show that the glial amino-acid transporter genderblind controls whether Drosophila melanogaster males will attempt to mate with other males. Genderblind (gb) mutant males showed no alteration in heterosexual courtship or copulation, but were attracted to normally unappealing male species-specific chemosensory cues. As a result, genderblind mutant males courted and attempted to copulate with other Drosophila males. This homosexual behavior could be induced within hours using inducible RNAi, suggesting that genderblind controls nervous system function rather than its development. Consistent with this, and indicating that glial genderblind regulates ambient extracellular glutamate to suppress glutamatergic synapse strength in vivo, homosexual behavior could be turned on and off by altering glutamatergic transmission pharmacologically and/or genetically.

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Figure 1: gb mutant males are 'genderblind'.
Figure 2: gb mutant males show altered responses to species-specific chemical sexual cues.
Figure 3: Genderblind (genderblind) protein is expressed in central glia surrounding glutamatergic neurons.
Figure 4: Drosophila male homosexual courtship is controlled by the strength of glutamatergic neurotransmission.

Change history

  • 16 December 2007

    In the version of this article originally published online, the title was incorrect. The correct title is "A glial amino-acid transporter controls synapse strength and courtship in Drosophila." This error has been corrected for all versions of the article.

  • 11 January 2008

    In the version of this article originally published online, the titles and captions of supplementary videos were missing. The error has been corrected online.

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Acknowledgements

We would like to thank P.-S. Ng for technical assistance, A. DiAntonio, T. Zars, R.F. Stocker, K. Broadie and H. for transgenic fly lines, W. Francke (University of Hamburg) for the synthesis of the 7-tricosene chemical, and B. Taylor (Oregon State) for helpful discussion and ideas. Other essential reagents were provided by the Drosophila Gene Disruption Project, the Vienna Drosophila RNAi Center and the Bloomington and Tucson Drosophila Stock Centers. Funding for this work was provided by grants from the Muscular Dystrophy Association and US National Institute of Neurological Disorders and Stroke (R01NS045628) to D.E.F., and by the Centre National de la Recherche Scientifique to J.-F.F.

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Author notes

  1. Yael Grosjean

    Present address: Present address: Center of Integrative Genomics, Genopode Building, Room 3033, University of Lausanne, CH-1015 Lausanne, Switzerland.,

Authors and Affiliations

  1. Biological Sciences, University of Illinois at Chicago, 840 W Taylor Street (MC 067), Chicago, Illinois, USA

    Yael Grosjean, Hrvoje Augustin & David E Featherstone

  2. Université de Bourgogne, UMR-5548 Centre National de la Recherche Scientifique 5548, 6 Boulevard Gabriel, Dijon, 21000, France

    Micheline Grillet & Jean-François Ferveur

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Contributions

Y.G. made the original observation that gb mutant males courted each other and was responsible for all genetic and pharmacological manipulations, immunohistochemistry and most of the behavioral experiments and analysis. M.G. was responsible for some locomotory tests, the heterosexual copulation measurements and the desat mutant male experiments and contributed to decapitated partner courtship tests. H.A. was responsible for the gb real-time RT-PCR and GB immunoblot data. D.E.F, Y.G. and J-F.F. were responsible for experimental design and interpretation of results and writing the article.

Corresponding author

Correspondence to David E Featherstone.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–4 (PDF 1956 kb)

Supplementary Video 1

This video shows six wild-type (Oregon R) males. They display little courtship behavior. (WMV 3057 kb)

Supplementary Video 2

This video shows six gb[KG07905] mutant males. They display frequent and extensive homosexual courtship behavior. (WMV 3047 kb)

Supplementary Video 3

This video shows six precise excision males (flies where the gb[KG07095] transposon has been precisely excised). They display very little courtship behavior. (WMV 3056 kb)

Supplementary Video 4

This video shows six males of the genotype TubGal4/UAS-DVGluT. In these flies, the Drosophila vesicular glutamate transporter DVGluT has been overexpressed to increase glutamatergic synapse strength. These flies display frequent and extensive homosexual courtship behavior. (WMV 1825 kb)

Supplementary Video 5

This video shows six gb[KG07095] mutant males that have drunk apple juice containing gamma-D-glutamylglycine (gamma-DGG), a competitive glutamate receptor antagonist that weakens glutamatergic synapse strength. These display very little courtship behavior. (WMV 244 kb)

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Grosjean, Y., Grillet, M., Augustin, H. et al. A glial amino-acid transporter controls synapse strength and courtship in Drosophila. Nat Neurosci 11, 54–61 (2008). https://doi.org/10.1038/nn2019

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