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The genetic architecture of odor-guided behavior in Drosophila: epistasis and the transcriptome

Nature Genetics volume 35, pages 180–184 (2003)Cite this article

Abstract

We combined transcriptional profiling and quantitative genetic analysis to elucidate the genetic architecture of olfactory behavior in Drosophila melanogaster. We applied whole-genome expression analysis to five coisogenic smell-impaired (smi) mutant lines and their control. We used analysis of variance to partition variation in transcript abundance between males and females and between smi genotypes and to determine the genotype-by-sex interaction. A total of 666 genes showed sexual dimorphism in transcript abundance, and 530 genes were coregulated in response to one or more smi mutations, showing considerable epistasis at the level of the transcriptome in response to single mutations. Quantitative complementation tests of mutations at these coregulated genes with the smi mutations showed that in most cases (67%) epistatic interactions for olfactory behavior mirrored epistasis at the level of transcription, thus identifying new candidate genes regulating olfactory behavior.

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Figure 1: Epistatic network of smi loci5.
Figure 2: 'Volcano plot' comparing P values for the 'sex' term from analysis of variance of transcript abundance for each probe set on the Affymetrix GeneChip and an arbitrary fold-change significance threshold.
Figure 3
Figure 4: Number of genes with altered expression in smi backgrounds.
Figure 5: Functional categories of genes with significantly altered transcript abundance in five smi lines and their control.

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References

  1. Mackay, T.F.C. The genetic architecture of quantitative traits. Annu. Rev. Genet. 35, 303–339 (2001).

    Article  CAS  Google Scholar 

  2. Sokolowski, M.B. Drosophila: genetics meets behaviour. Nat. Rev. Genet. 2, 879–890 (2001).

    Article  CAS  Google Scholar 

  3. Ideker, T., Galitski, T. & Hood, L. A new approach to decoding life: systems biology. Annu. Rev. Genomics Hum Genet. 2, 343–372 (2001).

    Article  CAS  Google Scholar 

  4. Anholt, R.R.H., Lyman, R.F. & Mackay, T.F.C. Effects of single P-element insertions on olfactory behavior in Drosophila melanogaster. Genetics 143, 293–301 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Fedorowicz, G.M., Fry, J.D., Anholt, R.R.H. & Mackay, T.F.C. Epistatic interactions between smell-impaired loci in Drosophila melanogaster. Genetics 148, 1885–1891 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Jin, W. et al. The contributions of sex, genotype and age to transcriptional variance in Drosophila melanogaster. Nat. Genet. 29, 389–395 (2001)

    Article  CAS  Google Scholar 

  7. Fujii, S. & Amrein, H. Genes expressed in the Drosophila head reveal a role for fat cells in sex-specific physiology. EMBO J. 21, 5353–5363 (2002).

    Article  CAS  Google Scholar 

  8. Wang, Q., Hasan, G. & Pikielny, C.W. Preferential expression of biotransformation enzymes in the olfactory organs of Drosophila melanogaster, the antennae. J. Biol. Chem. 274, 10309–10315 (1999).

    Article  CAS  Google Scholar 

  9. Galindo, K. & Smith, D.P. A large family of divergent Drosophila odorant-binding proteins expressed in gustatory and olfactory sensilla. Genetics 159, 1059–1072 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Hekmat-Scafe, D.S., Scafe, C.R., McKinney, A.J. & Tanouye, M.A. Genome-wide analysis of the odorant-binding protein gene family in Drosophila melanogaster. Genome Res. 12, 1357–1369 (2002).

    Article  CAS  Google Scholar 

  11. Kim, M.S., Repp, A. & Smith, D.P. LUSH odorant-binding protein mediates chemosensory responses to alcohols in Drosophila melanogaster. Genetics 150, 711–721 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Pikielny, C.W., Hasan, G., Rouyer, F. & Rosbash, M. Members of a family of Drosophila putative odorant-binding proteins are expressed in different subsets of olfactory hairs. Neuron 12, 35–49 (1994).

    Article  CAS  Google Scholar 

  13. Kulkarni, N.H., Yamamoto, A., Robinson, K.O., Mackay, T.F.C. & Anholt, R.R.H. The DSC1 channel, encoded by the smi60E locus, contributes to odor-guided behavior in Drosophila melanogaster. Genetics 161, 1507–1516 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Störtkuhl, K.F., Hovemann, B.T. & Carlson, J.R. Olfactory adaptation depends on the Trp Ca2+ channel in Drosophila. J. Neurosci. 19, 4839–4846 (1999).

    Article  Google Scholar 

  15. Vosshall, L.B., Wong, A.M. & Axel, R. An olfactory sensory map in the fly brain. Cell 102, 147–159 (2000).

    Article  CAS  Google Scholar 

  16. Hultmark, D. Drosophila immunity: paths and patterns. Curr. Opin. Immunol. 15, 12–19 (2003).

    Article  CAS  Google Scholar 

  17. Ganguly, I., Mackay, T.F.C. & Anholt, R.R.H. Scribble is essential for olfactory behavior in Drosophila melanogaster. Genetics, 164, 1447–1457 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Munier, A.I. et al. PVF2, a PDGF/VEGF-like growth factor, induces hemocyte proliferation in Drosophila larvae. EMBO Rep. 3, 1195–1200 (2002).

    Article  CAS  Google Scholar 

  19. Igakura, T. et al. Roles of basigin, a member of the immunoglobulin superfamily, in behavior as to an irritating odor, lymphocyte response, and blood-brain barrier. Biochem. Biophys. Res. Commun. 224, 33–36 (1996).

    Article  CAS  Google Scholar 

  20. Bilder, D. & Perrimon, N. Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature 403, 676–680 (2000).

    Article  CAS  Google Scholar 

  21. Bilder, D., Li, M. & Perrimon, N. Cooperative regulation of cell polarity and growth by Drosophila tumor suppressors. Science 289, 113–116 (2000).

    Article  CAS  Google Scholar 

  22. Roche, J.P., Packard, M.C., Moeckel-Cole, S. & Budnik, V. Regulation of synaptic plasticity and synaptic vesicle dynamics by the PDZ protein Scribble. J. Neurosci. 22, 6471–6479 (2002).

    Article  CAS  Google Scholar 

  23. Wu, L.P., Choe, K.M., Lu, Y. & Anderson, K.V. Drosophila immunity: genes on the third chromosome required for the response to bacterial infection. Genetics 159, 189–199 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Wang, J.W., Soll, D.R. & Wu, C.F. Morphometric description of the wandering behavior in Drosophila larvae: a phenotypic analysis of K+ channel mutants. J. Neurogenet. 16, 45–63 (2002).

    Article  CAS  Google Scholar 

  25. Raghavan, S. et al. Protein phosphatase 1β is required for the maintenance of muscle attachments. Curr. Biol. 10, 269–272 (2000).

    Article  CAS  Google Scholar 

  26. Tracey, W.D., Wilson, R.I., Laurent G. & Benzer, S. painless, a Drosophila gene essential for nociception. Cell 113, 261–273 (2003).

    Article  CAS  Google Scholar 

  27. Balakrishnan, R. & Rodrigues, V. The shaker and shaking-B genes specify elements in the processing of gustatory information in Drosophila melanogaster. J. Exp. Biol. 57, 161–181 (1991).

    Google Scholar 

  28. Kuniyoshi, H. et al. lingerer, a Drosophila gene involved in initiation and termination of copulation, encodes a set of novel cytoplasmic proteins. Genetics 162, 1775–1789 (2003).

    Google Scholar 

  29. Gaines, P., Tompkins, L., Woodard, C.T. & Carlson, J.R. quick-to-court, a Drosophila mutant with elevated levels of sexual behavior, is defective in a predicted coiled-coil protein. Genetics 154, 1627–1637 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Greenspan, R.J. The flexible genome. Nat. Rev. Genet. 2, 383–387 (2001).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the W. M. Keck Foundation and grants from the National Institutes of Health.

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Authors and Affiliations

  1. The Department of Zoology, North Carolina State University, Raleigh, 27695, North Carolina, USA

    Robert R H Anholt, Juan-José Fanara, Nalini H Kulkarni & Stephanie M Rollmann

  2. The Department of Genetics, North Carolina State University, Raleigh, 27695, North Carolina, USA

    Robert R H Anholt, Christy L Dilda, Juan-José Fanara, Indrani Ganguly & Trudy F C Mackay

  3. The W. M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, 27695, North Carolina, USA

    Robert R H Anholt, Juan-José Fanara, Nalini H Kulkarni, Indrani Ganguly, Stephanie M Rollmann & Trudy F C Mackay

  4. The Torrey Mesa Research Institute, La Jolla, California, USA

    Sherman Chang & Kim P Kamdar

  5. Department of Ecology, Genetics and Evolution, University of Buenos Aires, Buenos Aires, Argentina

    Juan-José Fanara

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  1. Robert R H Anholt
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Correspondence to Robert R H Anholt.

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Anholt, R., Dilda, C., Chang, S. et al. The genetic architecture of odor-guided behavior in Drosophila: epistasis and the transcriptome. Nat Genet 35, 180–184 (2003). https://doi.org/10.1038/ng1240

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