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Genetics. Feb 2000; 154(2): 725–745.
PMCID: PMC1460956

Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster.


The fruitless (fru) gene functions in Drosophila males to establish the potential for male sexual behaviors. fru encodes a complex set of sex-specific and sex-nonspecific mRNAs through the use of multiple promoters and alternative pre-mRNA processing. The male-specific transcripts produced from the distal (P1) fru promoter are believed to be responsible for its role in specifying sexual behavior and are only expressed in a small fraction of central nervous system (CNS) cells. To understand the molecular etiology of fruitless mutant phenotypes, we compared wild-type and mutant transcription patterns. These experiments revealed that the fru(2), fru(3), fru(4), and fru(sat) mutations, which are due to P-element inserts, alter the pattern of sex-specific and sex-nonspecific fru RNAs. These changes arise in part from the P-element insertions containing splice acceptor sites that create alternative processing pathways. In situ hybridization revealed no alterations in the locations of cells expressing the P1-fru-promoter-derived transcripts in fru(2), fru(3), fru(4), and fru(sat) pharate adults. For the fru(1) mutant (which is due to an inversion breakpoint near the P1 promoter), Northern analyses revealed no significant changes in fru transcript patterns. However, in situ hybridization revealed anomalies in the level and distribution of P1-derived transcripts: in fru(1) males, fewer P1-expressing neurons are found in regions of the dorsal lateral protocerebrum and abdominal ganglion compared to wild-type males. In other regions of the CNS, expression of these transcripts appears normal in fru(1) males. The loss of fruitless expression in these regions likely accounts for the striking courtship abnormalities exhibited by fru(1) males. Thus, we suggest that the mutant phenotypes in fru(2), fru(3), fru(4), and fru(sat) animals are due to a failure to appropriately splice P1 transcripts, whereas the mutant phenotype of fru(1) animals is due to the reduction or absence of P1 transcripts within specific regions of the CNS.

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Selected References

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  • Wilson WD, Tanious FA, Watson RA, Barton HJ, Strekowska A, Harden DB, Strekowski L. Interaction of unfused tricyclic aromatic cations with DNA: a new class of intercalators. Biochemistry. 1989 Mar 7;28(5):1984–1992. [PubMed]
  • Tanaka Y, Kimata K, Wake A, Mine S, Morimoto I, Yamakawa N, Habuchi H, Ashikari S, Yamamoto H, Sakurai K, et al. Heparan sulfate proteoglycan on leukemic cells is primarily involved in integrin triggering and its mediated adhesion to endothelial cells. J Exp Med. 1996 Nov 1;184(5):1987–1997. [PMC free article] [PubMed]
  • Hall JC. Portions of the central nervous system controlling reproductive behavior in Drosophila melanogaster. Behav Genet. 1977 Jul;7(4):291–312. [PubMed]
  • Hall JC. Control of male reproductive behavior by the central nervous system of Drosophila: dissection of a courtship pathway by genetic mosaics. Genetics. 1979 Jun;92(2):437–457. [PMC free article] [PubMed]
  • Hall JC. The mating of a fly. Science. 1994 Jun 17;264(5166):1702–1714. [PubMed]
  • Hazelrigg T, Levis R, Rubin GM. Transformation of white locus DNA in drosophila: dosage compensation, zeste interaction, and position effects. Cell. 1984 Feb;36(2):469–481. [PubMed]
  • Heinrichs V, Ryner LC, Baker BS. Regulation of sex-specific selection of fruitless 5' splice sites by transformer and transformer-2. Mol Cell Biol. 1998 Jan;18(1):450–458. [PMC free article] [PubMed]
  • Hing AL, Carlson JR. Male-male courtship behavior induced by ectopic expression of the Drosophila white gene: role of sensory function and age. J Neurobiol. 1996 Aug;30(4):454–464. [PubMed]
  • Horowitz H, Berg CA. Aberrant splicing and transcription termination caused by P element insertion into the intron of a Drosophila gene. Genetics. 1995 Jan;139(1):327–335. [PMC free article] [PubMed]
  • Hotta Y, Benzer S. Courtship in Drosophila mosaics: sex-specific foci for sequential action patterns. Proc Natl Acad Sci U S A. 1976 Nov;73(11):4154–4158. [PMC free article] [PubMed]
  • Hu S, Fambrough D, Atashi JR, Goodman CS, Crews ST. The Drosophila abrupt gene encodes a BTB-zinc finger regulatory protein that controls the specificity of neuromuscular connections. Genes Dev. 1995 Dec 1;9(23):2936–2948. [PubMed]
  • Ito H, Fujitani K, Usui K, Shimizu-Nishikawa K, Tanaka S, Yamamoto D. Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9687–9692. [PMC free article] [PubMed]
  • Moses K, Ellis MC, Rubin GM. The glass gene encodes a zinc-finger protein required by Drosophila photoreceptor cells. Nature. 1989 Aug 17;340(6234):531–536. [PubMed]
  • O'Connell PO, Rosbash M. Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene. Nucleic Acids Res. 1984 Jul 11;12(13):5495–5513. [PMC free article] [PubMed]
  • Pepling M, Mount SM. Sequence of a cDNA from the Drosophila melanogaster white gene. Nucleic Acids Res. 1990 Mar 25;18(6):1633–1633. [PMC free article] [PubMed]
  • Read D, Manley JL. Alternatively spliced transcripts of the Drosophila tramtrack gene encode zinc finger proteins with distinct DNA binding specificities. EMBO J. 1992 Mar;11(3):1035–1044. [PMC free article] [PubMed]
  • Albagli O, Dhordain P, Deweindt C, Lecocq G, Leprince D. The BTB/POZ domain: a new protein-protein interaction motif common to DNA- and actin-binding proteins. Cell Growth Differ. 1995 Sep;6(9):1193–1198. [PubMed]
  • Read D, Levine M, Manley JL. Ectopic expression of the Drosophila tramtrack gene results in multiple embryonic defects, including repression of even-skipped and fushi tarazu. Mech Dev. 1992 Sep;38(3):183–195. [PubMed]
  • Castrillon DH, Gönczy P, Alexander S, Rawson R, Eberhart CG, Viswanathan S, DiNardo S, Wasserman SA. Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: characterization of male-sterile mutants generated by single P element mutagenesis. Genetics. 1993 Oct;135(2):489–505. [PMC free article] [PubMed]
  • Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, Baker BS, Hall JC, Taylor BJ, Wasserman SA. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell. 1996 Dec 13;87(6):1079–1089. [PubMed]
  • Ferveur JF, Greenspan RJ. Courtship behavior of brain mosaics in Drosophila. J Neurogenet. 1998 Nov;12(4):205–226. [PubMed]
  • Taylor BJ, Villella A, Ryner LC, Baker BS, Hall JC. Behavioral and neurobiological implications of sex-determining factors in Drosophila. Dev Genet. 1994;15(3):275–296. [PubMed]
  • Tower J, Karpen GH, Craig N, Spradling AC. Preferential transposition of Drosophila P elements to nearby chromosomal sites. Genetics. 1993 Feb;133(2):347–359. [PMC free article] [PubMed]
  • Gailey DA, Taylor BJ, Hall JC. Elements of the fruitless locus regulate development of the muscle of Lawrence, a male-specific structure in the abdomen of Drosophila melanogaster adults. Development. 1991 Nov;113(3):879–890. [PubMed]
  • Villella A, Hall JC. Courtship anomalies caused by doublesex mutations in Drosophila melanogaster. Genetics. 1996 May;143(1):331–344. [PMC free article] [PubMed]
  • Villella A, Gailey DA, Berwald B, Ohshima S, Barnes PT, Hall JC. Extended reproductive roles of the fruitless gene in Drosophila melanogaster revealed by behavioral analysis of new fru mutants. Genetics. 1997 Nov;147(3):1107–1130. [PMC free article] [PubMed]
  • Yamamoto D, Ito H, Fujitani K. Genetic dissection of sexual orientation: behavioral, cellular, and molecular approaches in Drosophila melanogaster. Neurosci Res. 1996 Oct;26(2):95–107. [PubMed]
  • von Kalm L, Crossgrove K, Von Seggern D, Guild GM, Beckendorf SK. The Broad-Complex directly controls a tissue-specific response to the steroid hormone ecdysone at the onset of Drosophila metamorphosis. EMBO J. 1994 Aug 1;13(15):3505–3516. [PMC free article] [PubMed]
  • Yamamoto D, Fujitani K, Usui K, Ito H, Nakano Y. From behavior to development: genes for sexual behavior define the neuronal sexual switch in Drosophila. Mech Dev. 1998 May;73(2):135–146. [PubMed]
  • Wheeler DA, Kulkarni SJ, Gailey DA, Hall JC. Spectral analysis of courtship songs in behavioral mutants of Drosophila melanogaster. Behav Genet. 1989 Jul;19(4):503–528. [PubMed]
  • Zhang SD, Odenwald WF. Misexpression of the white (w) gene triggers male-male courtship in Drosophila. Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5525–5529. [PMC free article] [PubMed]
  • Wilson C, Pearson RK, Bellen HJ, O'Kane CJ, Grossniklaus U, Gehring WJ. P-element-mediated enhancer detection: an efficient method for isolating and characterizing developmentally regulated genes in Drosophila. Genes Dev. 1989 Sep;3(9):1301–1313. [PubMed]

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