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. 1994 Nov;138(3):721–732. doi: 10.1093/genetics/138.3.721

Dosage Compensation of the Period Gene in Drosophila Melanogaster

M K Cooper 1, M J Hamblen-Coyle 1, X Liu 1, J E Rutila 1, J C Hall 1
PMCID: PMC1206222  PMID: 7851769

Abstract

The period (per) gene is located on the X chromosome of Drosophila melanogaster. Its expression influences biological clocks in this fruit fly, including the one that subserves circadian rhythms of locomotor activity. Like most X-linked genes in Drosophila, per is under the regulatory control of gene dosage compensation. In this study, we assessed the activity of altered or augmented per(+) DNA fragments in transformants. Relative expression levels in male and female adults were inferred from periodicities associated with locomotor behavioral rhythms, and by histochemically assessing β-galactosidase levels in transgenics carrying different kinds of per-lacZ fusion genes. The results suggest that per contains multipartite regulatory information for dosage compensation within the large first intron and also within the 3' half of this genetic locus.

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Selected References

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  1. Baker B. S., Belote J. M. Sex determination and dosage compensation in Drosophila melanogaster. Annu Rev Genet. 1983;17:345–393. doi: 10.1146/annurev.ge.17.120183.002021. [DOI] [PubMed] [Google Scholar]
  2. Baylies M. K., Bargiello T. A., Jackson F. R., Young M. W. Changes in abundance or structure of the per gene product can alter periodicity of the Drosophila clock. 1987 Mar 26-Apr 1Nature. 326(6111):390–392. doi: 10.1038/326390a0. [DOI] [PubMed] [Google Scholar]
  3. Belote J. M., Lucchesi J. C. Control of X chromosome transcription by the maleless gene in Drosophila. Nature. 1980 Jun 19;285(5766):573–575. doi: 10.1038/285573a0. [DOI] [PubMed] [Google Scholar]
  4. Birchler J. A., Hiebert J. C., Paigen K. Analysis of autosomal dosage compensation involving the alcohol dehydrogenase locus in Drosophila melanogaster. Genetics. 1990 Mar;124(3):679–686. [PMC free article] [PubMed] [Google Scholar]
  5. Bowtell D. D., Lila T., Michael W. M., Hackett D., Rubin G. M. Analysis of the enhancer element that controls expression of sevenless in the developing Drosophila eye. Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6853–6857. doi: 10.1073/pnas.88.15.6853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Citri Y., Colot H. V., Jacquier A. C., Yu Q., Hall J. C., Baltimore D., Rosbash M. A family of unusually spliced biologically active transcripts encoded by a Drosophila clock gene. Nature. 1987 Mar 5;326(6108):42–47. doi: 10.1038/326042a0. [DOI] [PubMed] [Google Scholar]
  7. Colot H. V., Hall J. C., Rosbash M. Interspecific comparison of the period gene of Drosophila reveals large blocks of non-conserved coding DNA. EMBO J. 1988 Dec 1;7(12):3929–3937. doi: 10.1002/j.1460-2075.1988.tb03279.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Coté G. G., Brody S. Circadian rhythms in Drosophila melanogaster: analysis of period as a function of gene dosage at the per (period) locus. J Theor Biol. 1986 Aug 21;121(4):487–503. doi: 10.1016/s0022-5193(86)80104-7. [DOI] [PubMed] [Google Scholar]
  9. DOBZHANSKY T. [The X-chromosome in the larval salivary glands of hybrids Drosophila insularis x Drosophila tropicalis]. Chromosoma. 1957;8(6):691–698. doi: 10.1007/BF01259527. [DOI] [PubMed] [Google Scholar]
  10. Dushay M. S., Rosbash M., Hall J. C. Mapping the clock rhythm mutation to the period locus of Drosophila melanogaster by germline transformation. J Neurogenet. 1992 Sep;8(3):173–179. doi: 10.3109/01677069209083446. [DOI] [PubMed] [Google Scholar]
  11. Ewer J., Frisch B., Hamblen-Coyle M. J., Rosbash M., Hall J. C. Expression of the period clock gene within different cell types in the brain of Drosophila adults and mosaic analysis of these cells' influence on circadian behavioral rhythms. J Neurosci. 1992 Sep;12(9):3321–3349. doi: 10.1523/JNEUROSCI.12-09-03321.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Frisch B., Hardin P. E., Hamblen-Coyle M. J., Rosbash M., Hall J. C. A promoterless period gene mediates behavioral rhythmicity and cyclical per expression in a restricted subset of the Drosophila nervous system. Neuron. 1994 Mar;12(3):555–570. doi: 10.1016/0896-6273(94)90212-7. [DOI] [PubMed] [Google Scholar]
  13. Ghosh S., Chatterjee R. N., Bunick D., Manning J. E., Lucchesi J. C. The LSP1-alpha gene of Drosophila melanogaster exhibits dosage compensation when it is relocated to a different site on the X chromosome. EMBO J. 1989 Apr;8(4):1191–1196. doi: 10.1002/j.1460-2075.1989.tb03491.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ghosh S., Lucchesi J. C., Manning J. E. The non-dosage compensated LSP1-alpha gene of Drosophila melanogaster lies immediately downstream of the dosage compensated L12 gene. Mol Gen Genet. 1992 May;233(1-2):49–52. doi: 10.1007/BF00587560. [DOI] [PubMed] [Google Scholar]
  15. Gorman M., Kuroda M. I., Baker B. S. Regulation of the sex-specific binding of the maleless dosage compensation protein to the male X chromosome in Drosophila. Cell. 1993 Jan 15;72(1):39–49. doi: 10.1016/0092-8674(93)90048-u. [DOI] [PubMed] [Google Scholar]
  16. Graba Y., Aragnol D., Laurenti P., Garzino V., Charmot D., Berenger H., Pradel J. Homeotic control in Drosophila; the scabrous gene is an in vivo target of Ultrabithorax proteins. EMBO J. 1992 Sep;11(9):3375–3384. doi: 10.1002/j.1460-2075.1992.tb05416.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gutierrez A. G., Christensen A. C., Manning J. E., Lucchesi J. C. Cloning and dosage compensation of the 6-phosphogluconate dehydrogenase gene (Pgd+) of Drosophila melanogaster. Dev Genet. 1989;10(3):155–161. doi: 10.1002/dvg.1020100305. [DOI] [PubMed] [Google Scholar]
  18. Hall J. C., Kankel D. R. Genetics of acetylcholinesterase in Drosophila melanogaster. Genetics. 1976 Jul;83(3 PT2):517–535. [PMC free article] [PubMed] [Google Scholar]
  19. Hall J. C., Rosbash M. Genetic and molecular analysis of biological rhythms. J Biol Rhythms. 1987 Fall;2(3):153–178. doi: 10.1177/074873048700200301. [DOI] [PubMed] [Google Scholar]
  20. Hamblen-Coyle M., Konopka R. J., Zwiebel L. J., Colot H. V., Dowse H. B., Rosbash M., Hall J. C. A new mutation at the period locus of Drosophila melanogaster with some novel effects on circadian rhythms. J Neurogenet. 1989 Aug;5(4):229–256. doi: 10.3109/01677068909066210. [DOI] [PubMed] [Google Scholar]
  21. Hardin P. E., Hall J. C., Rosbash M. Circadian oscillations in period gene mRNA levels are transcriptionally regulated. Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11711–11715. doi: 10.1073/pnas.89.24.11711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hazelrigg T., Levis R., Rubin G. M. Transformation of white locus DNA in drosophila: dosage compensation, zeste interaction, and position effects. Cell. 1984 Feb;36(2):469–481. doi: 10.1016/0092-8674(84)90240-x. [DOI] [PubMed] [Google Scholar]
  23. Henikoff S., Meneely P. M. Unwinding dosage compensation. Cell. 1993 Jan 15;72(1):1–2. doi: 10.1016/0092-8674(93)90040-w. [DOI] [PubMed] [Google Scholar]
  24. Hiebert J. C., Birchler J. A. Effects of the maleless mutation on X and autosomal gene expression in Drosophila melanogaster. Genetics. 1994 Mar;136(3):913–926. doi: 10.1093/genetics/136.3.913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hiromi Y., Kuroiwa A., Gehring W. J. Control elements of the Drosophila segmentation gene fushi tarazu. Cell. 1985 Dec;43(3 Pt 2):603–613. doi: 10.1016/0092-8674(85)90232-6. [DOI] [PubMed] [Google Scholar]
  26. Jackson F. R., Bargiello T. A., Yun S. H., Young M. W. Product of per locus of Drosophila shares homology with proteoglycans. Nature. 1986 Mar 13;320(6058):185–188. doi: 10.1038/320185a0. [DOI] [PubMed] [Google Scholar]
  27. Konopka R. J., Benzer S. Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1971 Sep;68(9):2112–2116. doi: 10.1073/pnas.68.9.2112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Konopka R. J. Genetics of biological rhythms in Drosophila. Annu Rev Genet. 1987;21:227–236. doi: 10.1146/annurev.ge.21.120187.001303. [DOI] [PubMed] [Google Scholar]
  29. Korge G. Genetic analysis of the larval secretion gene Sgs-4 and its regulatory chromosome sites in Drosophila melanogaster. Chromosoma. 1981;84(3):373–390. doi: 10.1007/BF00286027. [DOI] [PubMed] [Google Scholar]
  30. Krishnan R., Swanson K. D., Ganguly R. Dosage compensation of a retina-specific gene in Drosophila miranda. Chromosoma. 1991 Feb;100(2):125–133. doi: 10.1007/BF00418246. [DOI] [PubMed] [Google Scholar]
  31. Krumm A., Roth G. E., Korge G. Transformation of salivary gland secretion protein gene Sgs-4 in Drosophila: stage- and tissue-specific regulation, dosage compensation, and position effect. Proc Natl Acad Sci U S A. 1985 Aug;82(15):5055–5059. doi: 10.1073/pnas.82.15.5055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kuroda M. I., Kernan M. J., Kreber R., Ganetzky B., Baker B. S. The maleless protein associates with the X chromosome to regulate dosage compensation in Drosophila. Cell. 1991 Sep 6;66(5):935–947. doi: 10.1016/0092-8674(91)90439-6. [DOI] [PubMed] [Google Scholar]
  33. Liu X., Lorenz L., Yu Q. N., Hall J. C., Rosbash M. Spatial and temporal expression of the period gene in Drosophila melanogaster. Genes Dev. 1988 Feb;2(2):228–238. doi: 10.1101/gad.2.2.228. [DOI] [PubMed] [Google Scholar]
  34. Liu X., Yu Q. A., Huang Z. S., Zwiebel L. J., Hall J. C., Rosbash M. The strength and periodicity of D. melanogaster circadian rhythms are differentially affected by alterations in period gene expression. Neuron. 1991 May;6(5):753–766. doi: 10.1016/0896-6273(91)90172-v. [DOI] [PubMed] [Google Scholar]
  35. Lucchesi J. C., Manning J. E. Gene dosage compensation in Drosophila melanogaster. Adv Genet. 1987;24:371–429. doi: 10.1016/s0065-2660(08)60013-9. [DOI] [PubMed] [Google Scholar]
  36. McNabb S. L., Beckendorf S. K. Cis-acting sequences which regulate expression of the Sgs-4 glue protein gene of Drosophila. EMBO J. 1986 Sep;5(9):2331–2340. doi: 10.1002/j.1460-2075.1986.tb04501.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Page T. L. Time is the essence: molecular analysis of the biological clock. Science. 1994 Mar 18;263(5153):1570–1572. doi: 10.1126/science.8128243. [DOI] [PubMed] [Google Scholar]
  38. Pirrotta V., Steller H., Bozzetti M. P. Multiple upstream regulatory elements control the expression of the Drosophila white gene. EMBO J. 1985 Dec 16;4(13A):3501–3508. doi: 10.1002/j.1460-2075.1985.tb04109.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Roberts D. B., Evans-Roberts S. The X-linked alpha-chain gene of Drosophila LSP-1 does not show dosage compensation. Nature. 1979 Aug 23;280(5724):691–692. doi: 10.1038/280691a0. [DOI] [PubMed] [Google Scholar]
  40. Rosbash M., Hall J. C. The molecular biology of circadian rhythms. Neuron. 1989 Oct;3(4):387–398. doi: 10.1016/0896-6273(89)90199-2. [DOI] [PubMed] [Google Scholar]
  41. Rutila J. E., Edery I., Hall J. C., Rosbash M. The analysis of new short-period circadian rhythm mutants suggests features of D. melanogaster period gene function. J Neurogenet. 1992 May;8(2):101–113. doi: 10.3109/01677069209084155. [DOI] [PubMed] [Google Scholar]
  42. Sass H., Meselson M. Dosage compensation of the Drosophila pseudoobscura Hsp82 gene and the Drosophila melanogaster Adh gene at ectopic sites in D. melanogaster. Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6795–6799. doi: 10.1073/pnas.88.15.6795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Scholnick S. B., Morgan B. A., Hirsh J. The cloned dopa decarboxylase gene is developmentally regulated when reintegrated into the Drosophila genome. Cell. 1983 Aug;34(1):37–45. doi: 10.1016/0092-8674(83)90134-4. [DOI] [PubMed] [Google Scholar]
  44. Scott M. J., Lucchesi J. C. Structure and expression of the Drosophila melanogaster gene encoding 6-phosphogluconate dehydrogenase. Gene. 1991 Dec 30;109(2):177–183. doi: 10.1016/0378-1119(91)90607-d. [DOI] [PubMed] [Google Scholar]
  45. Siwicki K. K., Eastman C., Petersen G., Rosbash M., Hall J. C. Antibodies to the period gene product of Drosophila reveal diverse tissue distribution and rhythmic changes in the visual system. Neuron. 1988 Apr;1(2):141–150. doi: 10.1016/0896-6273(88)90198-5. [DOI] [PubMed] [Google Scholar]
  46. Smith R. F., Konopka R. J. Circadian clock phenotypes of chromosome aberrations with a breakpoint at the per locus. Mol Gen Genet. 1981;183(2):243–251. doi: 10.1007/BF00270625. [DOI] [PubMed] [Google Scholar]
  47. Sokolove P. G., Bushell W. N. The chi square periodogram: its utility for analysis of circadian rhythms. J Theor Biol. 1978 May 8;72(1):131–160. doi: 10.1016/0022-5193(78)90022-x. [DOI] [PubMed] [Google Scholar]
  48. Spradling A. C., Rubin G. M. The effect of chromosomal position on the expression of the Drosophila xanthine dehydrogenase gene. Cell. 1983 Aug;34(1):47–57. doi: 10.1016/0092-8674(83)90135-6. [DOI] [PubMed] [Google Scholar]
  49. Wheeler D. A., Kyriacou C. P., Greenacre M. L., Yu Q., Rutila J. E., Rosbash M., Hall J. C. Molecular transfer of a species-specific behavior from Drosophila simulans to Drosophila melanogaster. Science. 1991 Mar 1;251(4997):1082–1085. doi: 10.1126/science.1900131. [DOI] [PubMed] [Google Scholar]
  50. Yu Q., Colot H. V., Kyriacou C. P., Hall J. C., Rosbash M. Behaviour modification by in vitro mutagenesis of a variable region within the period gene of Drosophila. Nature. 1987 Apr 23;326(6115):765–769. doi: 10.1038/326765a0. [DOI] [PubMed] [Google Scholar]
  51. Zehring W. A., Wheeler D. A., Reddy P., Konopka R. J., Kyriacou C. P., Rosbash M., Hall J. C. P-element transformation with period locus DNA restores rhythmicity to mutant, arrhythmic Drosophila melanogaster. Cell. 1984 Dec;39(2 Pt 1):369–376. doi: 10.1016/0092-8674(84)90015-1. [DOI] [PubMed] [Google Scholar]
  52. Zerr D. M., Hall J. C., Rosbash M., Siwicki K. K. Circadian fluctuations of period protein immunoreactivity in the CNS and the visual system of Drosophila. J Neurosci. 1990 Aug;10(8):2749–2762. doi: 10.1523/JNEUROSCI.10-08-02749.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]

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