Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1998 Oct;150(2):755–766. doi: 10.1093/genetics/150.2.755

Quantitative genetic analysis of copia retrotransposon activity in inbred Drosophila melanogaster lines.

S V Nuzhdin 1, E G Pasyukova 1, E A Morozova 1, A J Flavell 1
PMCID: PMC1460341  PMID: 9755206

Abstract

The rates of transcription and transposition of retrotransposons vary between lines of Drosophila melanogaster. We have studied the genetics of differences in copia retrotransposon activity by quantitative trait loci (QTL) mapping. Ninety-eight recombinant inbred lines were constructed from two parental lines exhibiting a 10-fold difference in copia transcript level and a 100-fold difference in transposition rate. The lines were scored for 126 molecular markers, copia transcript level, and rate of copia transposition. Transcript level correlated with copia copy number, and the difference in copia copy number between parental lines accounted for 45.1% of copia transcript-level difference. Most of the remaining difference was accounted for by two transcript-level QTL mapping to cytological positions 27B-30D and 50F-57C on the second chromosome, which accounted for 11.5 and 30.4%, respectively. copia transposition rate was controlled by interacting QTL mapping to the region 27B-48D on the second and 61A-65A and 97D-100A on the third chromosome. The genes controlling copia transcript level are thus not necessarily those involved in controlling copia transposition rate. Segregation of modifying genes, rather than mutations, might explain the variability in copia retrotransposon activity between lines.

Full Text

The Full Text of this article is available as a PDF (152.2 KB).

Selected References

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

  1. Bhadra U., Pal-Bhadra M., Birchler J. A. A sex-influenced modifier in Drosophila that affects a broad spectrum of target loci including the histone repeats. Genetics. 1997 Jul;146(3):903–917. doi: 10.1093/genetics/146.3.903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Birchler J. A., Hiebert J. C. Interaction of the Enhancer of white-apricot with transposable element alleles at the white locus in Drosophila melanogaster. Genetics. 1989 May;122(1):129–138. doi: 10.1093/genetics/122.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Biémont C., Aouar A., Arnault C. Genome reshuffling of the copia element in an inbred line of Drosophila melanogaster. Nature. 1987 Oct 22;329(6141):742–744. doi: 10.1038/329742a0. [DOI] [PubMed] [Google Scholar]
  4. Biémont C. Dynamic equilibrium between insertion and excision of P elements in highly inbred lines from an M' strain of Drosophila melanogaster. J Mol Evol. 1994 Nov;39(5):466–472. doi: 10.1007/BF00173415. [DOI] [PubMed] [Google Scholar]
  5. Biémont C., Lemeunier F., Garcia Guerreiro M. P., Brookfield J. F., Gautier C., Aulard S., Pasyukova E. G. Population dynamics of the copia, mdg1, mdg3, gypsy, and P transposable elements in a natural population of Drosophila melanogaster. Genet Res. 1994 Jun;63(3):197–212. doi: 10.1017/s0016672300032353. [DOI] [PubMed] [Google Scholar]
  6. Biémont C., Tsitrone A., Vieira C., Hoogland C. Transposable element distribution in Drosophila. Genetics. 1997 Dec;147(4):1997–1999. doi: 10.1093/genetics/147.4.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brookfield J. F., Badge R. M. Population genetics models of transposable elements. Genetica. 1997;100(1-3):281–294. [PubMed] [Google Scholar]
  8. Brookfield J. F. Models of repression of transposition in P-M hybrid dysgenesis by P cytotype and by zygotically encoded repressor proteins. Genetics. 1991 Jun;128(2):471–486. doi: 10.1093/genetics/128.2.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bucheton A., Lavige J. M., Picard G., L'Heritier P. Non-mendelian female sterility in Drosophila melanogaster: quantitative variations in the efficiency of inducer and reactive strains. Heredity (Edinb) 1976 Jun;36(3):305–314. doi: 10.1038/hdy.1976.38. [DOI] [PubMed] [Google Scholar]
  10. Bucheton A., Vaury C., Chaboissier M. C., Abad P., Pélisson A., Simonelig M. I elements and the Drosophila genome. Genetica. 1992;86(1-3):175–190. doi: 10.1007/BF00133719. [DOI] [PubMed] [Google Scholar]
  11. Cavarec L., Heidmann T. The Drosophila copia retrotransposon contains binding sites for transcriptional regulation by homeoproteins. Nucleic Acids Res. 1993 Nov 11;21(22):5041–5049. doi: 10.1093/nar/21.22.5041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cavarec L., Jensen S., Casella J. F., Cristescu S. A., Heidmann T. Molecular cloning and characterization of a transcription factor for the copia retrotransposon with homology to the BTB-containing lola neurogenic factor. Mol Cell Biol. 1997 Jan;17(1):482–494. doi: 10.1128/mcb.17.1.482. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cavarec L., Jensen S., Heidmann T. Identification of a strong transcriptional activator for the copia retrotransposon responsible for its differential expression in Drosophila hydei and melanogaster cell lines. Biochem Biophys Res Commun. 1994 Aug 30;203(1):392–399. doi: 10.1006/bbrc.1994.2195. [DOI] [PubMed] [Google Scholar]
  14. Charlesworth B., Jarne P., Assimacopoulos S. The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. III. Element abundances in heterochromatin. Genet Res. 1994 Dec;64(3):183–197. doi: 10.1017/s0016672300032845. [DOI] [PubMed] [Google Scholar]
  15. Charlesworth B., Langley C. H. The evolution of self-regulated transposition of transposable elements. Genetics. 1986 Feb;112(2):359–383. doi: 10.1093/genetics/112.2.359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Charlesworth B., Langley C. H. The population genetics of Drosophila transposable elements. Annu Rev Genet. 1989;23:251–287. doi: 10.1146/annurev.ge.23.120189.001343. [DOI] [PubMed] [Google Scholar]
  17. Charlesworth B., Lapid A. A study of ten families of transposable elements on X chromosomes from a population of Drosophila melanogaster. Genet Res. 1989 Oct;54(2):113–125. doi: 10.1017/s0016672300028482. [DOI] [PubMed] [Google Scholar]
  18. Charlesworth B., Lapid A., Canada D. The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. I. Element frequencies and distribution. Genet Res. 1992 Oct;60(2):103–114. doi: 10.1017/s0016672300030792. [DOI] [PubMed] [Google Scholar]
  19. Charlesworth B., Lapid A., Canada D. The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. II. Inferences on the nature of selection against elements. Genet Res. 1992 Oct;60(2):115–130. doi: 10.1017/s0016672300030809. [DOI] [PubMed] [Google Scholar]
  20. Charlesworth B., Sniegowski P., Stephan W. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature. 1994 Sep 15;371(6494):215–220. doi: 10.1038/371215a0. [DOI] [PubMed] [Google Scholar]
  21. Charlesworth B. Transposable elements in natural populations with a mixture of selected and neutral insertion sites. Genet Res. 1991 Apr;57(2):127–134. doi: 10.1017/s0016672300029190. [DOI] [PubMed] [Google Scholar]
  22. Csink A. K., Linsk R., Birchler J. A. Mosaic suppressor, a gene in Drosophila that modifies retrotransposon expression and interacts with zeste. Genetics. 1994 Feb;136(2):573–583. doi: 10.1093/genetics/136.2.573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Csink A. K., Linsk R., Birchler J. A. The Lighten up (Lip) gene of Drosophila melanogaster, a modifier of retroelement expression, position effect variegation and white locus insertion alleles. Genetics. 1994 Sep;138(1):153–163. doi: 10.1093/genetics/138.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Csink A. K., McDonald J. F. Analysis of copia sequence variation within and between Drosophila species. Mol Biol Evol. 1995 Jan;12(1):83–93. doi: 10.1093/oxfordjournals.molbev.a040193. [DOI] [PubMed] [Google Scholar]
  25. Csink A. K., McDonald J. F. copia expression is variable among natural populations of Drosophila. Genetics. 1990 Oct;126(2):375–385. doi: 10.1093/genetics/126.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Dombrádi V., Axton J. M., Glover D. M., Cohen P. T. Cloning and chromosomal localization of Drosophila cDNA encoding the catalytic subunit of protein phosphatase 1 alpha. High conservation between mammalian and insect sequences. Eur J Biochem. 1989 Aug 15;183(3):603–610. doi: 10.1111/j.1432-1033.1989.tb21089.x. [DOI] [PubMed] [Google Scholar]
  27. Eggleston W. B., Johnson-Schlitz D. M., Engels W. R. P-M hybrid dysgenesis does not mobilize other transposable element families in D. melanogaster. Nature. 1988 Jan 28;331(6154):368–370. doi: 10.1038/331368a0. [DOI] [PubMed] [Google Scholar]
  28. Finnegan D. J., Rubin G. M., Young M. W., Hogness D. S. Repeated gene families in Drosophila melanogaster. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):1053–1063. doi: 10.1101/sqb.1978.042.01.106. [DOI] [PubMed] [Google Scholar]
  29. Flavell A. J., Smith D. B., Kumar A. Extreme heterogeneity of Ty1-copia group retrotransposons in plants. Mol Gen Genet. 1992 Jan;231(2):233–242. doi: 10.1007/BF00279796. [DOI] [PubMed] [Google Scholar]
  30. Harada K., Yukuhiro K., Mukai T. Transposition rates of movable genetic elements in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1990 Apr;87(8):3248–3252. doi: 10.1073/pnas.87.8.3248. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Hiebert J. C., Birchler J. A. Dosage compensation of the copia retrotransposon in Drosophila melanogaster. Genetics. 1992 Mar;130(3):539–545. doi: 10.1093/genetics/130.3.539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hoogland C., Biémont C. Chromosomal distribution of transposable elements in Drosophila melanogaster: test of the ectopic recombination model for maintenance of insertion site number. Genetics. 1996 Sep;144(1):197–204. doi: 10.1093/genetics/144.1.197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kaplan N. L., Brookfield J. F. Transposable Elements in Mendelian Populations. III. Statistical Results. Genetics. 1983 Jul;104(3):485–495. doi: 10.1093/genetics/104.3.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Kazazian H. H., Jr, Wong C., Youssoufian H., Scott A. F., Phillips D. G., Antonarakis S. E. Haemophilia A resulting from de novo insertion of L1 sequences represents a novel mechanism for mutation in man. Nature. 1988 Mar 10;332(6160):164–166. doi: 10.1038/332164a0. [DOI] [PubMed] [Google Scholar]
  35. Kidwell M. G., Kidwell J. F., Sved J. A. Hybrid Dysgenesis in DROSOPHILA MELANOGASTER: A Syndrome of Aberrant Traits Including Mutation, Sterility and Male Recombination. Genetics. 1977 Aug;86(4):813–833. doi: 10.1093/genetics/86.4.813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kim A. I., Belyaeva E. S., Aslanian M. M. Autonomous transposition of gypsy mobile elements and genetic instability in Drosophila melanogaster. Mol Gen Genet. 1990 Nov;224(2):303–308. doi: 10.1007/BF00271566. [DOI] [PubMed] [Google Scholar]
  37. Kim A. I., Lyubomirskaya N. V., Belyaeva E. S., Shostack N. G., Ilyin Y. V. The introduction of a transpositionally active copy of retrotransposon GYPSY into the Stable Strain of Drosophila melanogaster causes genetic instability. Mol Gen Genet. 1994 Feb;242(4):472–477. doi: 10.1007/BF00281799. [DOI] [PubMed] [Google Scholar]
  38. Langley C. H., Montgomery E., Hudson R., Kaplan N., Charlesworth B. On the role of unequal exchange in the containment of transposable element copy number. Genet Res. 1988 Dec;52(3):223–235. doi: 10.1017/s0016672300027695. [DOI] [PubMed] [Google Scholar]
  39. Lohe A. R., Hartl D. L. Reduced germline mobility of a mariner vector containing exogenous DNA: effect of size or site? Genetics. 1996 Jul;143(3):1299–1306. doi: 10.1093/genetics/143.3.1299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Lohe A. R., Moriyama E. N., Lidholm D. A., Hartl D. L. Horizontal transmission, vertical inactivation, and stochastic loss of mariner-like transposable elements. Mol Biol Evol. 1995 Jan;12(1):62–72. doi: 10.1093/oxfordjournals.molbev.a040191. [DOI] [PubMed] [Google Scholar]
  41. Montgomery E. A., Huang S. M., Langley C. H., Judd B. H. Chromosome rearrangement by ectopic recombination in Drosophila melanogaster: genome structure and evolution. Genetics. 1991 Dec;129(4):1085–1098. doi: 10.1093/genetics/129.4.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Nuzhdin S. V., Mackay T. F. Direct determination of retrotransposon transposition rates in Drosophila melanogaster. Genet Res. 1994 Apr;63(2):139–144. doi: 10.1017/s0016672300032249. [DOI] [PubMed] [Google Scholar]
  43. Nuzhdin S. V., Mackay T. F. The genomic rate of transposable element movement in Drosophila melanogaster. Mol Biol Evol. 1995 Jan;12(1):180–181. doi: 10.1093/oxfordjournals.molbev.a040188. [DOI] [PubMed] [Google Scholar]
  44. Nuzhdin S. V., Pasyukova E. G., Dilda C. L., Zeng Z. B., Mackay T. F. Sex-specific quantitative trait loci affecting longevity in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1997 Sep 2;94(18):9734–9739. doi: 10.1073/pnas.94.18.9734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Nuzhdin S. V., Pasyukova E. G., Mackay T. F. Accumulation of transposable elements in laboratory lines of Drosophila melanogaster. Genetica. 1997;100(1-3):167–175. [PubMed] [Google Scholar]
  46. Nuzhdin S. V., Pasyukova E. G., Mackay T. F. Positive association between copia transposition rate and copy number in Drosophila melanogaster. Proc Biol Sci. 1996 Jul 22;263(1372):823–831. doi: 10.1098/rspb.1996.0122. [DOI] [PubMed] [Google Scholar]
  47. Nuzhdin S. V. The distribution of transposable elements on X chromosomes from a natural population of Drosophila simulans. Genet Res. 1995 Oct;66(2):159–166. doi: 10.1017/s0016672300034509. [DOI] [PubMed] [Google Scholar]
  48. Pasyukova E. G., Nuzhdin S. V. Doc and copia instability in an isogenic Drosophila melanogaster stock. Mol Gen Genet. 1993 Aug;240(2):302–306. doi: 10.1007/BF00277071. [DOI] [PubMed] [Google Scholar]
  49. Pasyukova E., Nuzhdin S., Li W., Flavell A. J. Germ line transposition of the copia retrotransposon in Drosophila melanogaster is restricted to males by tissue-specific control of copia RNA levels. Mol Gen Genet. 1997 Jun;255(1):115–124. doi: 10.1007/s004380050479. [DOI] [PubMed] [Google Scholar]
  50. Petrov D. A., Lozovskaya E. R., Hartl D. L. High intrinsic rate of DNA loss in Drosophila. Nature. 1996 Nov 28;384(6607):346–349. doi: 10.1038/384346a0. [DOI] [PubMed] [Google Scholar]
  51. Petrov D. A., Schutzman J. L., Hartl D. L., Lozovskaya E. R. Diverse transposable elements are mobilized in hybrid dysgenesis in Drosophila virilis. Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):8050–8054. doi: 10.1073/pnas.92.17.8050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Pélisson A., Song S. U., Prud'homme N., Smith P. A., Bucheton A., Corces V. G. Gypsy transposition correlates with the production of a retroviral envelope-like protein under the tissue-specific control of the Drosophila flamenco gene. EMBO J. 1994 Sep 15;13(18):4401–4411. doi: 10.1002/j.1460-2075.1994.tb06760.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Pélisson A., Teysset L., Chalvet F., Kim A., Prud'homme N., Terzian C., Bucheton A. About the origin of retroviruses and the co-evolution of the gypsy retrovirus with the Drosophila flamenco host gene. Genetica. 1997;100(1-3):29–37. [PubMed] [Google Scholar]
  54. Russ C. An Improved Method for Opsonic Index Estimations, involving the Separation of Red and White Human Blood Corpuscles. Proc R Soc Med. 1912;5(PATHOL):187–197. [PMC free article] [PubMed] [Google Scholar]
  55. Shrimpton A. E., Montgomery E. A., Langley C. H. OM Mutations in DROSOPHILA ANANASSAE Are Linked to Insertions of a Transposable Element. Genetics. 1986 Sep;114(1):125–135. doi: 10.1093/genetics/114.1.125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Silver J. Confidence limits for estimates of gene linkage based on analysis of recombinant inbred strains. J Hered. 1985 Nov-Dec;76(6):436–440. doi: 10.1093/oxfordjournals.jhered.a110140. [DOI] [PubMed] [Google Scholar]
  57. Sniegowski P. D., Charlesworth B. Transposable element numbers in cosmopolitan inversions from a natural population of Drosophila melanogaster. Genetics. 1994 Jul;137(3):815–827. doi: 10.1093/genetics/137.3.815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Wilson S., Matyunina L. V., McDonald J. F. An enhancer region within the copia untranslated leader contains binding sites for Drosophila regulatory proteins. Gene. 1998 Mar 16;209(1-2):239–246. doi: 10.1016/s0378-1119(98)00048-1. [DOI] [PubMed] [Google Scholar]
  59. Yoshioka K., Honma H., Zushi M., Kondo S., Togashi S., Miyake T., Shiba T. Virus-like particle formation of Drosophila copia through autocatalytic processing. EMBO J. 1990 Feb;9(2):535–541. doi: 10.1002/j.1460-2075.1990.tb08140.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Yun Y. D., Davis R. L. Copia RNA levels are elevated in dunce mutants and modulated by cAMP. Nucleic Acids Res. 1989 Oct 25;17(20):8313–8326. doi: 10.1093/nar/17.20.8313. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES