Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2002 Dec;162(4):1775–1789. doi: 10.1093/genetics/162.4.1775

lingerer, a Drosophila gene involved in initiation and termination of copulation, encodes a set of novel cytoplasmic proteins.

Hisato Kuniyoshi 1, Kotaro Baba 1, Ryu Ueda 1, Shunzo Kondo 1, Wakae Awano 1, Naoto Juni 1, Daisuke Yamamoto 1
PMCID: PMC1462391  PMID: 12524348

Abstract

In an effort to uncover genetic components underlying the courtship behavior of Drosophila melanogaster, we have characterized a novel gene, lingerer (lig), mutations of which result in abnormal copulation. Males carrying a hypomorphic mutation in lig fail to withdraw their genitalia upon termination of copulation, but display no overt abnormalities in their genitalia. A severe reduction in the dosage of the lig gene causes repeated attempted copulations but no successful copulations. Complete loss of lig function results in lethality during early pupal stages. lig is localized to polytene segment 44A on the second chromosome and encodes three alternatively spliced transcripts that generate two types of 150-kD proteins, Lig-A and Lig-B, differing only at the C terminus. Lig proteins show no similarity to known proteins. However, a set of homologous proteins in mammals suggest that Drosophila Lig belongs to a family of proteins that share five highly conserved domains. Lig is a cytoplasmic protein expressed in the central nervous system (CNS), imaginal discs, and gonads. Lig-A expression is selectively reduced in lig mutants and the ubiquitous supply of this protein at the beginning of metamorphosis restores the copulatory defects of the lig mutant. We propose that lig may act in the nervous system to mediate the control of copulatory organs during courtship.

Full Text

The Full Text of this article is available as a PDF (595.0 KB).

Selected References

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

  1. Baba K., Takeshita A., Majima K., Ueda R., Kondo S., Juni N., Yamamoto D. The Drosophila Bruton's tyrosine kinase (Btk) homolog is required for adult survival and male genital formation. Mol Cell Biol. 1999 Jun;19(6):4405–4413. doi: 10.1128/mcb.19.6.4405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bender M., Imam F. B., Talbot W. S., Ganetzky B., Hogness D. S. Drosophila ecdysone receptor mutations reveal functional differences among receptor isoforms. Cell. 1997 Dec 12;91(6):777–788. doi: 10.1016/s0092-8674(00)80466-3. [DOI] [PubMed] [Google Scholar]
  3. Bishop J. G., 3rd, Corces V. G. Expression of an activated ras gene causes developmental abnormalities in transgenic Drosophila melanogaster. Genes Dev. 1988 May;2(5):567–577. doi: 10.1101/gad.2.5.567. [DOI] [PubMed] [Google Scholar]
  4. Carlsson J., Drevin H., Axén R. Protein thiolation and reversible protein-protein conjugation. N-Succinimidyl 3-(2-pyridyldithio)propionate, a new heterobifunctional reagent. Biochem J. 1978 Sep 1;173(3):723–737. doi: 10.1042/bj1730723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ferveur J. F., Störtkuhl K. F., Stocker R. F., Greenspan R. J. Genetic feminization of brain structures and changed sexual orientation in male Drosophila. Science. 1995 Feb 10;267(5199):902–905. doi: 10.1126/science.7846534. [DOI] [PubMed] [Google Scholar]
  6. Finley K. D., Edeen P. T., Foss M., Gross E., Ghbeish N., Palmer R. H., Taylor B. J., McKeown M. Dissatisfaction encodes a tailless-like nuclear receptor expressed in a subset of CNS neurons controlling Drosophila sexual behavior. Neuron. 1998 Dec;21(6):1363–1374. doi: 10.1016/s0896-6273(00)80655-8. [DOI] [PubMed] [Google Scholar]
  7. Finley K. D., Taylor B. J., Milstein M., McKeown M. dissatisfaction, a gene involved in sex-specific behavior and neural development of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):913–918. doi: 10.1073/pnas.94.3.913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fletcher J. C., Burtis K. C., Hogness D. S., Thummel C. S. The Drosophila E74 gene is required for metamorphosis and plays a role in the polytene chromosome puffing response to ecdysone. Development. 1995 May;121(5):1455–1465. doi: 10.1242/dev.121.5.1455. [DOI] [PubMed] [Google Scholar]
  9. Gailey D. A., Hall J. C. Behavior and cytogenetics of fruitless in Drosophila melanogaster: different courtship defects caused by separate, closely linked lesions. Genetics. 1989 Apr;121(4):773–785. doi: 10.1093/genetics/121.4.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Greenspan R. J. Understanding the genetic construction of behavior. Sci Am. 1995 Apr;272(4):72–78. doi: 10.1038/scientificamerican0495-72. [DOI] [PubMed] [Google Scholar]
  11. Hall J. C. The mating of a fly. Science. 1994 Jun 17;264(5166):1702–1714. doi: 10.1126/science.8209251. [DOI] [PubMed] [Google Scholar]
  12. Hawkes R., Niday E., Gordon J. A dot-immunobinding assay for monoclonal and other antibodies. Anal Biochem. 1982 Jan 1;119(1):142–147. doi: 10.1016/0003-2697(82)90677-7. [DOI] [PubMed] [Google Scholar]
  13. Heinrichs V., Ryner L. C., Baker B. S. Regulation of sex-specific selection of fruitless 5' splice sites by transformer and transformer-2. Mol Cell Biol. 1998 Jan;18(1):450–458. doi: 10.1128/mcb.18.1.450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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. doi: 10.1073/pnas.93.18.9687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Juni N., Awasaki T., Yoshida K., Hori S. H. The Om (1E) mutation in Drosophila ananassae causes compound eye overgrowth due to tom retrotransposon-driven overexpression of a novel gene. Genetics. 1996 Jul;143(3):1257–1270. doi: 10.1093/genetics/143.3.1257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lehmann R., Tautz D. In situ hybridization to RNA. Methods Cell Biol. 1994;44:575–598. doi: 10.1016/s0091-679x(08)60933-4. [DOI] [PubMed] [Google Scholar]
  17. Nagase T., Kikuno R., Ishikawa K., Hirosawa M., Ohara O. Prediction of the coding sequences of unidentified human genes. XVII. The complete sequences of 100 new cDNA clones from brain which code for large proteins in vitro. DNA Res. 2000 Apr 28;7(2):143–150. doi: 10.1093/dnares/7.2.143. [DOI] [PubMed] [Google Scholar]
  18. Nagase T., Seki N., Tanaka A., Ishikawa K., Nomura N. Prediction of the coding sequences of unidentified human genes. IV. The coding sequences of 40 new genes (KIAA0121-KIAA0160) deduced by analysis of cDNA clones from human cell line KG-1. DNA Res. 1995 Aug 31;2(4):167-74, 199-210. doi: 10.1093/dnares/2.4.167. [DOI] [PubMed] [Google Scholar]
  19. Nakano Y., Fujitani K., Kurihara J., Ragan J., Usui-Aoki K., Shimoda L., Lukacsovich T., Suzuki K., Sezaki M., Sano Y. Mutations in the novel membrane protein spinster interfere with programmed cell death and cause neural degeneration in Drosophila melanogaster. Mol Cell Biol. 2001 Jun;21(11):3775–3788. doi: 10.1128/MCB.21.11.3775-3788.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rubin G. M., Spradling A. C. Genetic transformation of Drosophila with transposable element vectors. Science. 1982 Oct 22;218(4570):348–353. doi: 10.1126/science.6289436. [DOI] [PubMed] [Google Scholar]
  21. Ryner L. C., Goodwin S. F., Castrillon D. H., Anand A., Villella A., Baker B. S., Hall J. C., Taylor B. J., Wasserman S. A. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell. 1996 Dec 13;87(6):1079–1089. doi: 10.1016/s0092-8674(00)81802-4. [DOI] [PubMed] [Google Scholar]
  22. Steller H., Pirrotta V. P transposons controlled by the heat shock promoter. Mol Cell Biol. 1986 May;6(5):1640–1649. doi: 10.1128/mcb.6.5.1640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Taylor B. J., Villella A., Ryner L. C., Baker B. S., Hall J. C. Behavioral and neurobiological implications of sex-determining factors in Drosophila. Dev Genet. 1994;15(3):275–296. doi: 10.1002/dvg.1020150309. [DOI] [PubMed] [Google Scholar]
  24. Tower J., Karpen G. H., Craig N., Spradling A. C. Preferential transposition of Drosophila P elements to nearby chromosomal sites. Genetics. 1993 Feb;133(2):347–359. doi: 10.1093/genetics/133.2.347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Villella A., Gailey D. A., Berwald B., Ohshima S., Barnes P. T., Hall J. C. 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. doi: 10.1093/genetics/147.3.1107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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. doi: 10.1016/s0925-4773(98)00042-2. [DOI] [PubMed] [Google Scholar]
  27. 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. doi: 10.1016/s0168-0102(96)01087-5. [DOI] [PubMed] [Google Scholar]
  28. Yamamoto D., Jallon J. M., Komatsu A. Genetic dissection of sexual behavior in Drosophila melanogaster. Annu Rev Entomol. 1997;42:551–585. doi: 10.1146/annurev.ento.42.1.551. [DOI] [PubMed] [Google Scholar]
  29. Zhang P., Spradling A. C. Efficient and dispersed local P element transposition from Drosophila females. Genetics. 1993 Feb;133(2):361–373. doi: 10.1093/genetics/133.2.361. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES