Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1998 Apr;148(4):1885–1891. doi: 10.1093/genetics/148.4.1885

Epistatic interactions between smell-impaired loci in Drosophila melanogaster.

G M Fedorowicz 1, J D Fry 1, R R Anholt 1, T F Mackay 1
PMCID: PMC1460070  PMID: 9560402

Abstract

Odor-guided behavior is a polygenic trait determined by the concerted expression of multiple loci. Previously, P-element mutagenesis was used to identify single P[lArB] insertions, in a common isogenic background, with homozygous effects on olfactory behavior. Here, we have crossed 12 lines with these smell impaired (smi) mutations in a half-diallel design (excluding homozygous parental genotypes and reciprocal crosses) to produce all possible 66 doubly heterozygous hybrids with P[lArB] insertions at two distinct locations. The olfactory behavior of the transheterozygous progeny was measured using an assay that quantified the avoidance response to the repellent odorant benzaldehyde. There was significant variation in general combining abilities of avoidance scores among the smi mutants, indicating variation in heterozygous effects. Further, there was significant variation among specific combining abilities of each cross, indicating dependencies of heterozygous effects on the smi locus genotypes, i.e., epistasis. Significant epistatic interactions were identified for nine transheterozygote genotypes, involving 10 of the 12 smi loci. Eight of these loci form an interacting ensemble of genes that modulate expression of the behavioral phenotype. These observations illustrate the power of quantitative genetic analyses to detect subtle phenotypic effects and point to an extensive network of epistatic interactions among genes in the olfactory subgenome.

Full Text

The Full Text of this article is available as a PDF (109.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aceves-Piña E. O., Quinn W. G. Learning in normal and mutant Drosophila larvae. Science. 1979 Oct 5;206(4414):93–96. doi: 10.1126/science.206.4414.93. [DOI] [PubMed] [Google Scholar]
  2. Anholt R. R., Lyman R. F., Mackay T. F. Effects of single P-element insertions on olfactory behavior in Drosophila melanogaster. Genetics. 1996 May;143(1):293–301. doi: 10.1093/genetics/143.1.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Anholt R. R. Molecular neurobiology of olfaction. Crit Rev Neurobiol. 1993;7(1):1–22. [PubMed] [Google Scholar]
  4. Axel R. The molecular logic of smell. Sci Am. 1995 Oct;273(4):154–159. doi: 10.1038/scientificamerican1095-154. [DOI] [PubMed] [Google Scholar]
  5. Ayer R. K., Jr, Carlson J. Olfactory physiology in the Drosophila antenna and maxillary palp: acj6 distinguishes two classes of odorant pathways. J Neurobiol. 1992 Oct;23(8):965–982. doi: 10.1002/neu.480230804. [DOI] [PubMed] [Google Scholar]
  6. Belote J. M., McKeown M. B., Andrew D. J., Scott T. N., Wolfner M. F., Baker B. S. Control of sexual differentiation in Drosophila melanogaster. Cold Spring Harb Symp Quant Biol. 1985;50:605–614. doi: 10.1101/sqb.1985.050.01.073. [DOI] [PubMed] [Google Scholar]
  7. Botas J., Moscoso del Prado J., García-Bellido A. Gene-dose titration analysis in the search of trans-regulatory genes in Drosophila. EMBO J. 1982;1(3):307–310. doi: 10.1002/j.1460-2075.1982.tb01165.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Buck L. B. Information coding in the vertebrate olfactory system. Annu Rev Neurosci. 1996;19:517–544. doi: 10.1146/annurev.ne.19.030196.002505. [DOI] [PubMed] [Google Scholar]
  9. Fadool D. A., Ache B. W. Plasma membrane inositol 1,4,5-trisphosphate-activated channels mediate signal transduction in lobster olfactory receptor neurons. Neuron. 1992 Nov;9(5):907–918. doi: 10.1016/0896-6273(92)90243-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Helfand S. L., Carlson J. R. Isolation and characterization of an olfactory mutant in Drosophila with a chemically specific defect. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2908–2912. doi: 10.1073/pnas.86.8.2908. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Homyk T., Jr, Emerson C. P., Jr Functional interactions between unlinked muscle genes within haploinsufficient regions of the Drosophila genome. Genetics. 1988 May;119(1):105–121. doi: 10.1093/genetics/119.1.105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kennison J. A., Russell M. A. Dosage-Dependent Modifiers of Homoeotic Mutations in Drosophila melanogaster. Genetics. 1987 May;116(1):75–86. doi: 10.1093/genetics/116.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lilly M., Carlson J. smellblind: a gene required for Drosophila olfaction. Genetics. 1990 Feb;124(2):293–302. doi: 10.1093/genetics/124.2.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lilly M., Kreber R., Ganetzky B., Carlson J. R. Evidence that the Drosophila olfactory mutant smellblind defines a novel class of sodium channel mutation. Genetics. 1994 Mar;136(3):1087–1096. doi: 10.1093/genetics/136.3.1087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Long A. D., Mullaney S. L., Mackay T. F., Langley C. H. Genetic interactions between naturally occurring alleles at quantitative trait loci and mutant alleles at candidate loci affecting bristle number in Drosophila melanogaster. Genetics. 1996 Dec;144(4):1497–1510. doi: 10.1093/genetics/144.4.1497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lyman R. F., Lawrence F., Nuzhdin S. V., Mackay T. F. Effects of single P-element insertions on bristle number and viability in Drosophila melanogaster. Genetics. 1996 May;143(1):277–292. doi: 10.1093/genetics/143.1.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mackay T. F., Fry J. D. Polygenic mutation in Drosophila melanogaster: genetic interactions between selection lines and candidate quantitative trait loci. Genetics. 1996 Oct;144(2):671–688. doi: 10.1093/genetics/144.2.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mackay T. F., Hackett J. B., Lyman R. F., Wayne M. L., Anholt R. R. Quantitative genetic variation of odor-guided behavior in a natural population of Drosophila melanogaster. Genetics. 1996 Oct;144(2):727–735. doi: 10.1093/genetics/144.2.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mackay T. F., Lyman R. F., Jackson M. S. Effects of P element insertions on quantitative traits in Drosophila melanogaster. Genetics. 1992 Feb;130(2):315–332. doi: 10.1093/genetics/130.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. McKenna M., Monte P., Helfand S. L., Woodard C., Carlson J. A simple chemosensory response in Drosophila and the isolation of acj mutants in which it is affected. Proc Natl Acad Sci U S A. 1989 Oct;86(20):8118–8122. doi: 10.1073/pnas.86.20.8118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Riesgo-Escovar J., Raha D., Carlson J. R. Requirement for a phospholipase C in odor response: overlap between olfaction and vision in Drosophila. Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2864–2868. doi: 10.1073/pnas.92.7.2864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sengupta P., Chou J. H., Bargmann C. I. odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell. 1996 Mar 22;84(6):899–909. doi: 10.1016/s0092-8674(00)81068-5. [DOI] [PubMed] [Google Scholar]
  23. Troemel E. R., Chou J. H., Dwyer N. D., Colbert H. A., Bargmann C. I. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell. 1995 Oct 20;83(2):207–218. doi: 10.1016/0092-8674(95)90162-0. [DOI] [PubMed] [Google Scholar]
  24. Vihtelic T. S., Goebl M., Milligan S., O'Tousa J. E., Hyde D. R. Localization of Drosophila retinal degeneration B, a membrane-associated phosphatidylinositol transfer protein. J Cell Biol. 1993 Sep;122(5):1013–1022. doi: 10.1083/jcb.122.5.1013. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES