Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 2003 May;164(1):173–186. doi: 10.1093/genetics/164.1.173

Logjam encodes a predicted EMP24/GP25 protein that is required for Drosophila oviposition behavior.

Ginger E Carney 1, Barbara J Taylor 1
PMCID: PMC1462565  PMID: 12750330

Abstract

A newly characterized Drosophila melanogaster gene, logjam (loj), functions in female reproduction by modulating oviposition behavior. The locus encodes at least six overlapping transcripts with unique 5' ends. P-element mutants that express very low levels of loj transcripts are unable to oviposit mature eggs. This phenotype can be rescued by the introduction of a transgene expressing the most abundant loj transcript. As for many genes that specify behavioral outputs, loj is present in the adult central nervous system (CNS). Interestingly, it is also observed in vitellogenic egg chambers, suggesting that there may be multiple functions for this gene in egg-laying behavior. loj encodes a predicted protein with homology to the EMP24/GP25 transmembrane components of cytoplasmic vesicles and likely functions in intracellular trafficking.

Full Text

The Full Text of this article is available as a PDF (515.3 KB).

Selected References

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

  1. Adams M. D., Celniker S. E., Holt R. A., Evans C. A., Gocayne J. D., Amanatides P. G., Scherer S. E., Li P. W., Hoskins R. A., Galle R. F. The genome sequence of Drosophila melanogaster. Science. 2000 Mar 24;287(5461):2185–2195. doi: 10.1126/science.287.5461.2185. [DOI] [PubMed] [Google Scholar]
  2. Ahmad Shaad M., Baker Bruce S. Sex-specific deployment of FGF signaling in Drosophila recruits mesodermal cells into the male genital imaginal disc. Cell. 2002 May 31;109(5):651–661. doi: 10.1016/s0092-8674(02)00744-4. [DOI] [PubMed] [Google Scholar]
  3. Aigaki T., Fleischmann I., Chen P. S., Kubli E. Ectopic expression of sex peptide alters reproductive behavior of female D. melanogaster. Neuron. 1991 Oct;7(4):557–563. doi: 10.1016/0896-6273(91)90368-a. [DOI] [PubMed] [Google Scholar]
  4. Baker B. S., Ridge K. A. Sex and the single cell. I. On the action of major loci affecting sex determination in Drosophila melanogaster. Genetics. 1980 Feb;94(2):383–423. doi: 10.1093/genetics/94.2.383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Belden W. J., Barlowe C. Erv25p, a component of COPII-coated vesicles, forms a complex with Emp24p that is required for efficient endoplasmic reticulum to Golgi transport. J Biol Chem. 1996 Oct 25;271(43):26939–26946. doi: 10.1074/jbc.271.43.26939. [DOI] [PubMed] [Google Scholar]
  6. Boggs R. T., Gregor P., Idriss S., Belote J. M., McKeown M. Regulation of sexual differentiation in D. melanogaster via alternative splicing of RNA from the transformer gene. Cell. 1987 Aug 28;50(5):739–747. doi: 10.1016/0092-8674(87)90332-1. [DOI] [PubMed] [Google Scholar]
  7. Burtis K. C., Coschigano K. T., Baker B. S., Wensink P. C. The doublesex proteins of Drosophila melanogaster bind directly to a sex-specific yolk protein gene enhancer. EMBO J. 1991 Sep;10(9):2577–2582. doi: 10.1002/j.1460-2075.1991.tb07798.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Burtis K. C. The regulation of sex determination and sexually dimorphic differentiation in Drosophila. Curr Opin Cell Biol. 1993 Dec;5(6):1006–1014. doi: 10.1016/0955-0674(93)90085-5. [DOI] [PubMed] [Google Scholar]
  9. Carney G. E., Bender M. The Drosophila ecdysone receptor (EcR) gene is required maternally for normal oogenesis. Genetics. 2000 Mar;154(3):1203–1211. doi: 10.1093/genetics/154.3.1203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cavener D. R., Ray S. C. Eukaryotic start and stop translation sites. Nucleic Acids Res. 1991 Jun 25;19(12):3185–3192. doi: 10.1093/nar/19.12.3185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chapman T., Herndon L. A., Heifetz Y., Partridge L., Wolfner M. F. The Acp26Aa seminal fluid protein is a modulator of early egg hatchability in Drosophila melanogaster. Proc Biol Sci. 2001 Aug 22;268(1477):1647–1654. doi: 10.1098/rspb.2001.1684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chen P. S., Stumm-Zollinger E., Aigaki T., Balmer J., Bienz M., Böhlen P. A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster. Cell. 1988 Jul 29;54(3):291–298. doi: 10.1016/0092-8674(88)90192-4. [DOI] [PubMed] [Google Scholar]
  13. Ciufo L. F., Boyd A. Identification of a lumenal sequence specifying the assembly of Emp24p into p24 complexes in the yeast secretory pathway. J Biol Chem. 2000 Mar 24;275(12):8382–8388. doi: 10.1074/jbc.275.12.8382. [DOI] [PubMed] [Google Scholar]
  14. Cline T. W., Meyer B. J. Vive la différence: males vs females in flies vs worms. Annu Rev Genet. 1996;30:637–702. doi: 10.1146/annurev.genet.30.1.637. [DOI] [PubMed] [Google Scholar]
  15. D'Avino P. P., Thummel C. S. Ectopic expression systems in Drosophila. Methods Enzymol. 1999;306:129–142. doi: 10.1016/s0076-6879(99)06009-7. [DOI] [PubMed] [Google Scholar]
  16. Denzel A., Otto F., Girod A., Pepperkok R., Watson R., Rosewell I., Bergeron J. J., Solari R. C., Owen M. J. The p24 family member p23 is required for early embryonic development. Curr Biol. 2000 Jan 13;10(1):55–58. doi: 10.1016/s0960-9822(99)00266-3. [DOI] [PubMed] [Google Scholar]
  17. Dubnau J., Tully T. Gene discovery in Drosophila: new insights for learning and memory. Annu Rev Neurosci. 1998;21:407–444. doi: 10.1146/annurev.neuro.21.1.407. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. Fleischmann I., Cotton B., Choffat Y., Spengler M., Kubli E. Mushroom bodies and post-mating behaviors of Drosophila melanogaster females. J Neurogenet. 2001;15(2):117–144. doi: 10.3109/01677060109066198. [DOI] [PubMed] [Google Scholar]
  21. Füllekrug J., Suganuma T., Tang B. L., Hong W., Storrie B., Nilsson T. Localization and recycling of gp27 (hp24gamma3): complex formation with other p24 family members. Mol Biol Cell. 1999 Jun;10(6):1939–1955. doi: 10.1091/mbc.10.6.1939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Goodwin S. F., Taylor B. J., Villella A., Foss M., Ryner L. C., Baker B. S., Hall J. C. Aberrant splicing and altered spatial expression patterns in fruitless mutants of Drosophila melanogaster. Genetics. 2000 Feb;154(2):725–745. doi: 10.1093/genetics/154.2.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Heifetz Y., Lung O., Frongillo E. A., Jr, Wolfner M. F. The Drosophila seminal fluid protein Acp26Aa stimulates release of oocytes by the ovary. Curr Biol. 2000 Jan 27;10(2):99–102. doi: 10.1016/s0960-9822(00)00288-8. [DOI] [PubMed] [Google Scholar]
  25. Heifetz Y., Tram U., Wolfner M. F. Male contributions to egg production: the role of accessory gland products and sperm in Drosophila melanogaster. Proc Biol Sci. 2001 Jan 22;268(1463):175–180. doi: 10.1098/rspb.2000.1347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Karpen G. H., Spradling A. C. Analysis of subtelomeric heterochromatin in the Drosophila minichromosome Dp1187 by single P element insertional mutagenesis. Genetics. 1992 Nov;132(3):737–753. doi: 10.1093/genetics/132.3.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Keisman E. L., Baker B. S. The Drosophila sex determination hierarchy modulates wingless and decapentaplegic signaling to deploy dachshund sex-specifically in the genital imaginal disc. Development. 2001 May;128(9):1643–1656. doi: 10.1242/dev.128.9.1643. [DOI] [PubMed] [Google Scholar]
  29. Keisman E. L., Christiansen A. E., Baker B. S. The sex determination gene doublesex regulates the A/P organizer to direct sex-specific patterns of growth in the Drosophila genital imaginal disc. Dev Cell. 2001 Aug;1(2):215–225. doi: 10.1016/s1534-5807(01)00027-2. [DOI] [PubMed] [Google Scholar]
  30. Liu Y., Krantz D. E., Waites C., Edwards R. H. Membrane trafficking of neurotransmitter transporters in the regulation of synaptic transmission. Trends Cell Biol. 1999 Sep;9(9):356–363. doi: 10.1016/s0962-8924(99)01605-0. [DOI] [PubMed] [Google Scholar]
  31. Lupas A., Van Dyke M., Stock J. Predicting coiled coils from protein sequences. Science. 1991 May 24;252(5009):1162–1164. doi: 10.1126/science.252.5009.1162. [DOI] [PubMed] [Google Scholar]
  32. Manning A. Corpus allatum and sexual receptivity in female Drosophila melanogaster. Nature. 1966 Sep 17;211(5055):1321–1322. doi: 10.1038/2111321b0. [DOI] [PubMed] [Google Scholar]
  33. Manning A. The control of sexual receptivity in female Drosophila. Anim Behav. 1967 Apr-Jul;15(2):239–250. doi: 10.1016/0003-3472(67)90006-1. [DOI] [PubMed] [Google Scholar]
  34. Marzioch M., Henthorn D. C., Herrmann J. M., Wilson R., Thomas D. Y., Bergeron J. J., Solari R. C., Rowley A. Erp1p and Erp2p, partners for Emp24p and Erv25p in a yeast p24 complex. Mol Biol Cell. 1999 Jun;10(6):1923–1938. doi: 10.1091/mbc.10.6.1923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. McKeown M., Belote J. M., Boggs R. T. Ectopic expression of the female transformer gene product leads to female differentiation of chromosomally male Drosophila. Cell. 1988 Jun 17;53(6):887–895. doi: 10.1016/s0092-8674(88)90369-8. [DOI] [PubMed] [Google Scholar]
  36. McKeown M. Sex determination and differentiation. Dev Genet. 1994;15(3):201–204. doi: 10.1002/dvg.1020150302. [DOI] [PubMed] [Google Scholar]
  37. Monastirioti M., Linn C. E., Jr, White K. Characterization of Drosophila tyramine beta-hydroxylase gene and isolation of mutant flies lacking octopamine. J Neurosci. 1996 Jun 15;16(12):3900–3911. doi: 10.1523/JNEUROSCI.16-12-03900.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Monsma S. A., Wolfner M. F. Structure and expression of a Drosophila male accessory gland gene whose product resembles a peptide pheromone precursor. Genes Dev. 1988 Sep;2(9):1063–1073. doi: 10.1101/gad.2.9.1063. [DOI] [PubMed] [Google Scholar]
  39. Nagoshi R. N., McKeown M., Burtis K. C., Belote J. M., Baker B. S. The control of alternative splicing at genes regulating sexual differentiation in D. melanogaster. Cell. 1988 Apr 22;53(2):229–236. doi: 10.1016/0092-8674(88)90384-4. [DOI] [PubMed] [Google Scholar]
  40. 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]
  41. Robertson H. M., Preston C. R., Phillis R. W., Johnson-Schlitz D. M., Benz W. K., Engels W. R. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics. 1988 Mar;118(3):461–470. doi: 10.1093/genetics/118.3.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Rothman J. E., Wieland F. T. Protein sorting by transport vesicles. Science. 1996 Apr 12;272(5259):227–234. doi: 10.1126/science.272.5259.227. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. Saudan Philippe, Hauck Klaus, Soller Matthias, Choffat Yves, Ottiger Michael, Spörri Michael, Ding Zhaobing, Hess Daniel, Gehrig Peter M., Klauser Stefan. Ductus ejaculatorius peptide 99B (DUP99B), a novel Drosophila melanogaster sex-peptide pheromone. Eur J Biochem. 2002 Feb;269(3):989–997. doi: 10.1046/j.0014-2956.2001.02733.x. [DOI] [PubMed] [Google Scholar]
  45. Schekman R., Orci L. Coat proteins and vesicle budding. Science. 1996 Mar 15;271(5255):1526–1533. doi: 10.1126/science.271.5255.1526. [DOI] [PubMed] [Google Scholar]
  46. Schimmöller F., Singer-Krüger B., Schröder S., Krüger U., Barlowe C., Riezman H. The absence of Emp24p, a component of ER-derived COPII-coated vesicles, causes a defect in transport of selected proteins to the Golgi. EMBO J. 1995 Apr 3;14(7):1329–1339. doi: 10.1002/j.1460-2075.1995.tb07119.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Sokolowski M. B. Drosophila: genetics meets behaviour. Nat Rev Genet. 2001 Nov;2(11):879–890. doi: 10.1038/35098592. [DOI] [PubMed] [Google Scholar]
  48. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997 Dec 15;25(24):4876–4882. doi: 10.1093/nar/25.24.4876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Thompson K. J., Roosevelt J. L. Comparison of neural elements in sexually dimorphic segments of the grasshopper, Schistocerca americana. J Comp Neurol. 1998 Apr 27;394(1):14–28. [PubMed] [Google Scholar]
  50. Tompkins L. Genetic analysis of sex appeal in Drosophila. Behav Genet. 1984 Sep;14(5):411–440. doi: 10.1007/BF01065443. [DOI] [PubMed] [Google Scholar]
  51. 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]
  52. Villella A., Hall J. C. Courtship anomalies caused by doublesex mutations in Drosophila melanogaster. Genetics. 1996 May;143(1):331–344. doi: 10.1093/genetics/143.1.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Waterbury J. A., Jackson L. L., Schedl P. Analysis of the doublesex female protein in Drosophila melanogaster: role on sexual differentiation and behavior and dependence on intersex. Genetics. 1999 Aug;152(4):1653–1667. doi: 10.1093/genetics/152.4.1653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Wolfner M. F., Harada H. A., Bertram M. J., Stelick T. J., Kraus K. W., Kalb J. M., Lung Y. O., Neubaum D. M., Park M., Tram U. New genes for male accessory gland proteins in Drosophila melanogaster. Insect Biochem Mol Biol. 1997 Oct;27(10):825–834. doi: 10.1016/s0965-1748(97)00056-8. [DOI] [PubMed] [Google Scholar]
  55. Wolfner M. F. The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila. Heredity (Edinb) 2002 Feb;88(2):85–93. doi: 10.1038/sj.hdy.6800017. [DOI] [PubMed] [Google Scholar]
  56. Wolfner M. F. Tokens of love: functions and regulation of Drosophila male accessory gland products. Insect Biochem Mol Biol. 1997 Mar;27(3):179–192. doi: 10.1016/s0965-1748(96)00084-7. [DOI] [PubMed] [Google Scholar]
  57. 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]
  58. Yeo S. L., Lloyd A., Kozak K., Dinh A., Dick T., Yang X., Sakonju S., Chia W. On the functional overlap between two Drosophila POU homeo domain genes and the cell fate specification of a CNS neural precursor. Genes Dev. 1995 May 15;9(10):1223–1236. doi: 10.1101/gad.9.10.1223. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES