Journal of Molecular Evolution

, Volume 42, Issue 4, pp 392–408 | Cite as

Mutational mechanisms, phylogeny, and evolution of a repetitive region within a clock gene ofDrosophila melanogaster

  • E. Rosato
  • A. A. Peixoto
  • A. Gallippi
  • C. P. Kyriacou
  • R. Costa
Articles

Abstract

TheD. melanogaster clock geneperiod (per) is an internally repetitive gene encoding a tandem array of Thr-Gly codons that are highly polymorphic in length in European natural populations. The two major length variants, (Thr-Gly)20 and (Thr-Gly)17, show a highly significant latitudinal cline. In this study we present the complete sequence of the Thr-Gly region of 91 individuals from 6 natural populations ofD. melanogaster, 5 from Europe and 1 from North Africa. We further characterized these 91 individuals for polymorphic sites in two other regions, one upstream and one downstream of the Thr-Gly repeat. We used the haplotypic combinations of Thr-Gly allele with flanking markers in an attempt to identify the mechanisms involved in the evolution of theD. melanogaster Thr-Gly region and to infer the phylogenetic relationship existing among the Thr-Gly alleles. We observe evidence for both intra- and interallelic mutational mechanisms, including replication slippage, unequal crossing-over, and gene conversion.

Key words

D. melanogaster period gene Repetitive DNA Molecular phylogeny 

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References

  1. Anderson PR, Oakeshott JG (1984) Parallel geographical patterns of allozyme variation in two siblingDrosophila species. Nature 308:729–731CrossRefGoogle Scholar
  2. Andersson S, Lambertsson A (1993) Evolution of thedec-1 eggshell locus inDrosophila. II. Intraspecific DNA sequence analysis reveals length mutations in a repetitive region inD. melanogaster. J Mol Evol 36:536–544PubMedCrossRefGoogle Scholar
  3. Aquadro CF (1992) Why is the genome variable? Insights fromDrosophila. Trends Genet 8:355–362PubMedGoogle Scholar
  4. Aquadro CF (1993) Molecular population genetics ofDrosophila. In: Oakeshott J, Whitten MJ (eds) Molecular approaches to fundamental and applied entomology. Springer Verlag, Berlin, pp 222–226Google Scholar
  5. Aronson BD, Johnson KA, Dunlap JC (1994) Circadian clock locusfrequency: protein encoded by a single open reading frame defines period length and temperature compensation. Proc Natl Acad Sci USA 91:7683–7687PubMedCrossRefGoogle Scholar
  6. Berry A, Kreitman M (1993) Molecular analysis of an allozyme cline:Alcohol dehydrogenase inDrosophila melanogaster on the east coast of North America. Genetics 134:869–893PubMedGoogle Scholar
  7. Burbach KM, Poland A, Bradfield CA (1992) Cloning of the Ahreceptor cDNA reveals a distinctive ligand-activated transcription factor. Proc Natl Acad Sci USA 89:8185–8189PubMedCrossRefGoogle Scholar
  8. Castiglione-Morelli MA, Guantieri V, Villani V, Kyriacou CP, Costa R, Tamburro AM (1995) Conformational study of the Thr-Gly repeat in theDrosophila clock protein period. Proc R Soc Lond [Biol] 260:155–163Google Scholar
  9. Charlesworth B, Sniegowski P, Stephen W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220PubMedCrossRefGoogle Scholar
  10. Citri Y, Colot HV, Jacquier AC, Yu Q, Hall JC, Baltimore D, Rosbash M (1987) A family of unusually spliced biologically active transcripts encoded by aDrosophila clock gene. Nature 326:42–47PubMedCrossRefGoogle Scholar
  11. Costa R, Peixoto AA, Thackeray JR, Dalgleish R, Kyriacou CP (1991) Length polymorphism in the Threonine-Glycine encoding repeat region of theperiod gene inDrosophila. J Mol Evol 32:238–246PubMedCrossRefGoogle Scholar
  12. Costa R, Peixoto AA, Barbujani G, Kyriacou CP (1992) A latitudinal cline in aDrosophila clock gene. Proc R Soc Lond Biol 250:43–49Google Scholar
  13. David JR, Bocquet C (1975) Similarities and differences in latitudinal adaptation of twoDrosophila sibling species. Nature 257:588–590PubMedCrossRefGoogle Scholar
  14. David JR, Capy P (1988) Genetic variation ofDrosophila melanogaster natural populations. Trends Genet 4:106–111PubMedCrossRefGoogle Scholar
  15. Djian P, Phillips M, Easley K, Huang E, Simon M, Rice RH, Green H (1993) The involucrin genes of the mouse and the rat: study of their shared repeats. Mol Biol Evol 10:1136–1149PubMedGoogle Scholar
  16. Dover GA (1982) Molecular drive: cohesive mode of species evolution. Nature 299:111–117PubMedCrossRefGoogle Scholar
  17. Dover GA (1986) Molecular drive in multigene families: how biological novelties arise, spread and are assimilated. Trends Genet 2:159–165CrossRefGoogle Scholar
  18. Dover GA (1987) DNA turnover and the molecular clock. J Mol Evol 26:47–58PubMedCrossRefGoogle Scholar
  19. Dover GA (1989) Slips, strings and species. Trends Genet 5:100–103PubMedCrossRefGoogle Scholar
  20. Eickbush TH, Burke WD (1986) The silkmoth late chorion locus II. Gradients of gene conversion in two paired multigene families. J Mol Biol 190:357–366PubMedCrossRefGoogle Scholar
  21. Ewer J, Hamblen-Coyle M, Rosbash M, Hall JC (1990) Requirement forperiod gene expression in the adult and not during development for locomotor activity rhythms of imaginalDrosophila melanogaster. J Neurogenet 7:31–73PubMedGoogle Scholar
  22. Gloor G, Engels W (1990) Single-fly DNA preps for PCR.Drosophila Information Newsletter vol 1, January 1990Google Scholar
  23. Goodbourn SEY, Higgs DR, Clegg JB, Weatherall DJ (1983) Molecular basis of length polymorphism in the human ζ-globin complex. Proc Natl Acad Sci USA 80:5022–5026PubMedCrossRefGoogle Scholar
  24. Green H, Djian P (1992) Consecutive actions of different gene-altering mechanisms in the evolution of involucrin. Mol Biol Evol 9:977–1017PubMedGoogle Scholar
  25. Harding RM, Boyce AJ, Clegg JB (1992) The evolution of tandemly repetitive DNA: recombination rules. Genetics 132:847–859PubMedGoogle Scholar
  26. Hickey DA (1982) Selfish DNA. A sexually-transmitted nuclear parasite. Genetics 101:519–531PubMedGoogle Scholar
  27. Hilliker AJ, Harauz G, Reaume AG, Gray M, Clark SH, Chovnick A (1994) Meiotic gene conversion tract length distribution within therosy locus ofDrosophila melanogaster. Genetics 137:1019–1026PubMedGoogle Scholar
  28. Hoffman EC, Reyes H, Chu F-F, Sander F, Conley LH, Brooks BA Hankinson O (1991) Cloning of a factor required for activity of the Ah (dioxin) receptor. Science 252:954–958PubMedCrossRefGoogle Scholar
  29. Hoffmann AA, Parsons PA (1993) Direct and correlated responses to selection for desiccation resistance: a comparison ofD. melanogaster andD. simulans. J Evol Biol 6:643–657CrossRefGoogle Scholar
  30. Housman D (1995) Gain of glutamines, gain of function? Nature Genet 10:3–4PubMedCrossRefGoogle Scholar
  31. Howard J (1995) Not all converted yet. Nat Genet 10:371–373PubMedCrossRefGoogle Scholar
  32. Huang JH, Edery L, Rosbash M (1993) PAS is a dimerization domain common toDrosophila period and several transcriptional factors. Nature 364:359–362CrossRefGoogle Scholar
  33. Huang ZJ, Curtin KD, Rosbash M (1995)period protein intra- and inter-molecular interactions contribute to temperature compensation of a circadian clock inDrosophila. Neuron 14:365–372PubMedCrossRefGoogle Scholar
  34. Jackson FR, Bargiello TA, Yun S-H, Young MW (1986) Product of theper locus ofDrosophila shares homology with proteoglycans. Nature 320:185–188PubMedCrossRefGoogle Scholar
  35. Jeffreys AJ, Wilson V, Thein SL (1985) Hypervariable ‘minisatellite’ regions in human DNA. Nature 314:67–73PubMedCrossRefGoogle Scholar
  36. Jeffreys AJ, Royle NJ, Wilson V, Wong Z (1988a) Spontaneous mutation rates to new length alleles at tandem-repetitive hypervariable loci in human DNA. Nature 332:278–281PubMedCrossRefGoogle Scholar
  37. Jeffreys AJ, Wilson V, Neumann R, Keyte J (1988b) Amplification of human minisatellites by polymerase chain reaction: towards DNA fingerprinting of single cells. Nucleic Acids Res 16:10953–10971PubMedGoogle Scholar
  38. Jeffreys AJ, Neumann R, Wilson V (1990) Repeat unit sequence variation in minisatellites: a novel source of DNA polymorphism for studying variation and mutation by single molecule analysis. Cell 60:473–485PubMedCrossRefGoogle Scholar
  39. Jeffreys AJ, Monckton DG, Tamaki K, Neil DL, Armour JAL, MacLeod A, Collick A, Allen M, Jobling M (1993) Minisatellite variant mapping: application to DNA typing and mutation analysis. In: Pena SDJ, Chakraborty R, Epplen JT, Jeffreys AJ (eds) DNA fingerprinting: state of the science. Birkhauser Verlag, Basel, pp 125–139Google Scholar
  40. Jeffreys AJ, Tamaki K, McLeod A, Monckton DG, Neil DL, Armour JAL (1994) Complex gene conversion events in germline mutation at human minisatellites. Nat Genet 6:136–145PubMedCrossRefGoogle Scholar
  41. Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, CambridgeGoogle Scholar
  42. Konopka RJ, Benzer S (1971) Clock mutants ofDrosophila melanogaster. Proc Natl Acad Sci USA 68:2112–2116PubMedCrossRefGoogle Scholar
  43. Kreitman M (1991) Detecting selection at the level of DNA. In: Selander RK, Clarck AG, Whittam TS (eds) Evolution at the molecular level. Sinauer, Sunderland, MA, pp 204–221Google Scholar
  44. Kyriacou CP, Hall JC (1986) Interspecific genetic control of courtship song production and reception inDrosophila. Science 232:494–497PubMedCrossRefGoogle Scholar
  45. Levinson G, Gutman GA (1987) Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 4:203–221PubMedGoogle Scholar
  46. Matsui M, Mitsui Y, Ishida N (1994) Circadian regulation ofper repeat mRNA in the suprachiasmatic nucleus of rat brain. Neurosci Lett 163:189–192CrossRefGoogle Scholar
  47. McClung CR, Fox BA, Dunlap JC (1989)frequency, a clock gene inNeurospora shares a sequence element with theDrosophila clock geneperiod. Nature 339:558–562PubMedCrossRefGoogle Scholar
  48. Mitsui K, Yaguchi S, Tsurugi K (1994) TheGTS1 gene, which contains a Gly-Thr repeat, affects the timing of budding and cell size of the yeastSaccharomyces cerevisiae. Mol Cell Biol 14:5569–5578PubMedGoogle Scholar
  49. Muskavitch MAT, Hogness DS (1982) An expandable gene that encodes aDrosophila glue protein is not expressed in variants lacking remote upstream sequences. Cell 29:1041–1051PubMedCrossRefGoogle Scholar
  50. Nambu JR, Lewis JO, Wharton KA Crews ST (1991) TheDrosophila single minded gene encodes a helix-loop-helix protein that acts as a master regulator of CNS midline development. Cell 67:1157–1167PubMedCrossRefGoogle Scholar
  51. Nielsen J, Peixoto AA, Piccin A, Costa R, Kyriacou CP, Chalmers D (1994) Big flies, small repeats: the “Thr-Gly” region of theperiod gene inDiptera. Mol Biol Evol 11:839–853PubMedGoogle Scholar
  52. Peixoto A (1993) Molecular evolution of a repetitive region within a clock gene inDrosophila. Ph D thesisGoogle Scholar
  53. Peixoto AA, Campesan S, Costa R, Kyriacou CP (1993) Molecular evolution of a repetitive region within theper gene ofDrosophila. Mol Biol Evol 10:127–139PubMedGoogle Scholar
  54. Peixoto AA, Costa R, Wheeler DA, Hall JC, Kyriacou CP (1992) Evolution of the Threonine-Glycine repeat region of theperiod gene in themelanogaster species subgroup ofDrosophila. J Mol Evol 35:711–719CrossRefGoogle Scholar
  55. Perutz MF, Johnson T, Suzuki M, Finch JT (1994) Glutamine repeats as polar zippers: their possible role in inherited neurodegenerative diseases. Proc Natl Acad USA 991:5355–5338CrossRefGoogle Scholar
  56. Richards RI, Sutherland GR (1992) Dynamic mutations: a new class of mutations causing human disease. Cell 70:709–712PubMedCrossRefGoogle Scholar
  57. Rosato E, Peixoto AA, Barbujani G, Costa R, Kyriacou CP (1994) Molecular polymorphism in theperiod gene ofDrosophila simulans. Genetics 138:693–707PubMedGoogle Scholar
  58. Strand M, Prolla TA, Liskay RM, Petes TD (1993) Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature 365:274–276PubMedCrossRefGoogle Scholar
  59. Tautz D (1989) Hypervariability of simple sequences as a general source for DNA markers. Nucleic Acid Res 17:6463–6471PubMedGoogle Scholar
  60. Wheeler DA, Kyriacou CP, Greenacre M, Yu Q, Rutila J, Rosbash M, Hall JC (1991) Molecular transfer of a species-specific courtship behaviour fromDrosophila simulans toDrosophila melanogaster. Science 251:1082–1085PubMedCrossRefGoogle Scholar
  61. Yu Q, Colot HV, Kyriacou CP, Hall JC, Rosbash M (1987) Behaviour modification by in vitro mutagenesis of a variable region within theperiod gene ofDrosophila. Nature 326:765–769PubMedCrossRefGoogle Scholar
  62. Zangenberg G, Huang M, Arnheim N, Erlich H (1995) New HLA-DPB1 alleles generated by interallelic gene conversion detected by analysis of sperm. Nat Genet 10:407–414PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 1996

Authors and Affiliations

  • E. Rosato
    • 1
    • 2
  • A. A. Peixoto
    • 1
  • A. Gallippi
    • 2
  • C. P. Kyriacou
    • 1
  • R. Costa
    • 2
    • 3
  1. 1.Department of GeneticsUniversity of LeicesterLeicesterUK
  2. 2.Dipartimento di BiologiaUniversita' di PadovaPadovaItaly
  3. 3.Dipartimento di BiologiaUniversita' di LecceLecceItaly

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