Male-specific expression of the Fruitless protein is not common to all Drosophila species
Abstract
Sex-specific behavioral patterns must be a result of sexual differences in the structure and/or function of the central nervous system (CNS). Male Drosophila melanogaster mutants for the fruitless (fru) locus exhibit enhanced male-to-male courtship. The fru mutant males are accompanied by malformation of the male-specific muscle of Lawrence (MOL), which, in wild-type males, is induced by male motoneurons innervating it. These two phenotypes are the consequences of impaired sex determination of CNS neurons. In D. melanogaster, although the fru mRNAs are transcribed in the CNS of both the male and female, the Fru protein is only translated in the male CNS. This male-specific translation of Fru was also observed in D. simulans, D. yakuba, D. pseudoobscura and D. virilis; however, in D. suzukii, the Fru protein expression was detected even in the female CNS.
Key words
central nervous system fruitless sex determination Transformer translational controlPreview
Unable to display preview. Download preview PDF.
References
- Baba, K., A. Takeshita, K. Majima, R. Ueda, S. Kondo, N. Juni & D. Yamamoto, 1999. The Dwsophila Bruton’s tyrosine kinase (Btk) homolog is required for adult survival and male genital formation. Mol. Cell. Biol. 19: 4405–1413.Google Scholar
- Bashaw, G.J. & B.S. Baker, 1997. The regulation of the Dwsophila msl-2 gene reveals a function for Sex-lethal in translational control. Cell 89: 789–798.PubMedCrossRefGoogle Scholar
- Charlesworth, B., 1996. The evolution of chromosomal sex determination and dosage compensation. Curr. Biol. 6: 149–162.PubMedCrossRefGoogle Scholar
- Gailey, D.A., S. Ohshima, S.J. Santiago, J.M. Montez, A.R. Arellano, J. Robillo, C.A. Villarimo, L. Roberts, E. Fine, A. Villella & J.C. Hall, 1997. The muscle of Iawrence in Drosophila: a case of repeated evolutionary loss. P. Natl. Acad. Sci. USA 96: 4543–4547CrossRefGoogle Scholar
- Goodwin, S.F., B.J. Taylor, A. Villella, M. Foss, L.C. Ryner, B.S. Baker & J.C. Hall, 2000. Aberrant splicing and altered spatial expression patterns in fruitless mutants of Dwsophila melanogaster. Genetics 154: 725–745.PubMedGoogle Scholar
- Heinrichs, V, L.C. Ryner & B. Baker, 1998. Regulation of sexspecific selection of fruitless 5 splice sites by transformer and transformer-2. Mol. Cell. Biol. 18: 450–458.PubMedGoogle Scholar
- Hotta, Y.& S. Benzer, 1976. Courtship in Dwsophila mosaics: sexspecific foci for sequential action patterns. P. Natl. Acad. Sci. USA 73: 4154–4158.CrossRefGoogle Scholar
- Ito, H., K. Fujitani, K. Usui, K. Shimizu-Nishikawa, S. Tanaka & D. Yamamoto, 1996. Sexual orientation in Dwsophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. P. Natl. Acad. Sci. USA 93: 9687–9692.CrossRefGoogle Scholar
- Kelley, R.L., J. Wang, L. Bell & M.I. Kuroda, 1997. Sex lethal controls dosage compensation in Drosophila by a nonsplicing mechanism.Nature 387: 195–199.PubMedCrossRefGoogle Scholar
- Kimura, K.I., K. Usui & T. Tanimura, 1994. Female myoblasts can participate in the formation of a male-specific muscle in Drosophila. Zool. Sci. 11: 247–251.Google Scholar
- Lawrence, P.A. & P. Johnston, 1986. The muscle pattern of a segment of Drosophila may be determined by neurons and not by contributing myoblasts. Cell 45: 505–513.PubMedCrossRefGoogle Scholar
- Lee, G. & J.C. Hall, 2001. Abnormalities of male-specific FRU protein and serotonin expression in the CNS of fruitless mutants in Drosophila. J. Neurosci. 15: 513–526.Google Scholar
- Lee, G., M. Foss, S.F. Goodwin, T. Carlo, B.J. Taylor & J.C. Hall, 2000. Spatial, temporal, and sexually dimorphic expression patterns of the fruitless gene in the Drosophila central nervous system. J. Neurobiol. 43: 404–426.PubMedCrossRefGoogle Scholar
- Marin, I. & B.S. Baker, 1998. The evolutionary dynamics of sex determination. Science 281: 1990–1994.PubMedCrossRefGoogle Scholar
- Merendino, L., S. Guth, D. Bilbao, C. Martínez & J. Valcárcel, 1999. Inhibition of msl-2 splicing by Sex-lethal reveals interaction between U2AF35 and the 3 splice site AG. Nature 402: 838–841.PubMedCrossRefGoogle Scholar
- Nakano, Y, K. Fujitani, J. Kurihara, J. Ragan, K. Usui-Aoki, L. Shimoda, T. Lukacsovich, K. Suzuki, M. Sezaki, Y. Sano, R. Ueda, W. Awano, M. Kaneda, M. Umeda & D. Yamamoto, 2001. Mutations in the novel membrane protein spinster interfere with programmed cell death and cause neural degeneration in Drosophila melanogaster. Mol. Cell. Biol. 21: 3775–3788.PubMedCrossRefGoogle Scholar
- Parkes, T.L., A.J. Elia, D. Dickinson, A.J. Hilliker, J.R. Phillips & G.L. Boulianne, 1998. Extension of Drosophila lifespan by overexpression of human SODI in motorneurons. Nat. Genet. 19: 171–174.Google Scholar
- Ryner, L.C., S.F. Goodwin, D.H. Castrillon, A. Anand, A. Villella, B.S. Baker, J.C. Hall, B.J. Taylor & S.A. Wasserman, 1996. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87: 1079–1089.PubMedCrossRefGoogle Scholar
- Usui-Aoki, K., H. Ito, K. Ui-Tei, K. Takahashi, T. Lukacsovich, W. Awano, H. Nakata, Z.F. Piao, E.E. Nilsson, J. Tomida & D. Yamamoto, 2000. Formation of the male-specific muscle in female Drosophila by ectopic fruitless expression. Nat. Cell Biol. 2: 500–506.PubMedCrossRefGoogle Scholar
- Yamamoto, D. & Y. Nakano, 1999. Sexual behavior mutants revisited: molecular and cellular basis of Drosophila mating. Cell. Mol. Life Sci. 56: 634–646.PubMedCrossRefGoogle Scholar
- Yamamoto, D., K. Fujitani, K. Usui, H. Ito & Y. Nakano, 1998. From behavior to development: genes for sexual behav ior define the neuronal sexual switch in Drosophila. Mech. Dev. 73: 135–146.PubMedCrossRefGoogle Scholar
- Yokokura, T., R. Ueda & D. Yamamoto, 1995. Phenotypic and molecular characterization of croaker, a new mating behavior mutant of Drosophila melanogaster. Jpn. J. Genet. 70: 103–117.PubMedCrossRefGoogle Scholar
- Zollman, S., D. Godt, G.G. Prive, J.-L. Coudrec & F.A. Laski, 1994. The BTB domain, found primarily in zinc finger proteins, defines an evolutionarily conserved family that includes several developmentally regulated genes in Drosophila. P. Natl. Acad. Sci. USA 91: 10717–10721.CrossRefGoogle Scholar