Abstract
Multigene families on the Y chromosome face an unusual array of evolutionary forces. Both ribosomal DNA and Stellate, the two families examined here, have multiple copies of similar sequences on the X and Y chromosomes. Although the rate of sequence divergence on the Y chromosome depends on rates of mutation, gene conversion and exchange with the X chromosome, as well as purifying selection, the regulation of gene copy number may also depend on other pleiotropic functions, such as maintenance of chromosome pairing. Gene copy numbers were estimated for a series of 34 Y chromosome replacement lines using densitometric measurements of slot blots of genomic DNA from adult Drosophila melanogaster. Scans of autoradiographs of the same blots probed with the cloned alcohol dehydrogenase gene, a single copy gene, served as internal standards. Copy numbers span a 6-fold range for ribosomal DNA and a 3-fold range for Stellate DNA. Despite this magnitude of variation, there was no association between copy number and segregation variation of the sex chromosomes.
Full text
PDF![1944](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/d1fe/286821/f1d3a4c66ec1/pnas00246-0212.png)
![1945](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/d1fe/286821/ae6d88bba0d2/pnas00246-0213.png)
![1946](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/d1fe/286821/636d347de604/pnas00246-0214.png)
![1947](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/d1fe/286821/cab863a2f81b/pnas00246-0215.png)
![1948](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/d1fe/286821/04c73004a07e/pnas00246-0216.png)
Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Appels R., Hilliker A. J. The cytogenetic boundaries of the rDNA region within heterochromatin in the X chromosome of Drosophila melanogaster and their relation to male meiotic pairing sites. Genet Res. 1982 Apr;39(2):149–156. doi: 10.1017/s001667230002084x. [DOI] [PubMed] [Google Scholar]
- Atwood K. C. Some aspects of the bobbed problem in Drosophila. Genetics. 1969;61(1 Suppl):319–327. [PubMed] [Google Scholar]
- Buescher P. J., Phillips R. L., Brambl R. Ribosomal RNA contents of maize genotypes with different ribosomal RNA gene numbers. Biochem Genet. 1984 Oct;22(9-10):923–930. doi: 10.1007/BF00499483. [DOI] [PubMed] [Google Scholar]
- Burke W. D., Calalang C. C., Eickbush T. H. The site-specific ribosomal insertion element type II of Bombyx mori (R2Bm) contains the coding sequence for a reverse transcriptase-like enzyme. Mol Cell Biol. 1987 Jun;7(6):2221–2230. doi: 10.1128/mcb.7.6.2221. [DOI] [PMC free article] [PubMed] [Google Scholar]
- COOPER K. W. MEIOTIC CONJUNCTIVE ELEMENTS NOT INVOLVING CHIASMATA. Proc Natl Acad Sci U S A. 1964 Nov;52:1248–1255. doi: 10.1073/pnas.52.5.1248. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clark A. G., Lyckegaard E. M. Natural selection with nuclear and cytoplasmic transmission. III. Joint analysis of segregation and mtDNA in Drosophila melanogaster. Genetics. 1988 Mar;118(3):471–481. doi: 10.1093/genetics/118.3.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clark A. G. Natural selection and Y-linked polymorphism. Genetics. 1987 Mar;115(3):569–577. doi: 10.1093/genetics/115.3.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clark A. G. Variation in Y chromosome segregation in natural populations of Drosophila melanogaster. Genetics. 1987 Jan;115(1):143–151. doi: 10.1093/genetics/115.1.143. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cluster P. D., Marinković D., Allard R. W., Ayala F. J. Correlations between development rates, enzyme activities, ribosomal DNA spacer-length phenotypes, and adaptation in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1987 Jan;84(2):610–614. doi: 10.1073/pnas.84.2.610. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Coen E. S., Dover G. A. Unequal exchanges and the coevolution of X and Y rDNA arrays in Drosophila melanogaster. Cell. 1983 Jul;33(3):849–855. doi: 10.1016/0092-8674(83)90027-2. [DOI] [PubMed] [Google Scholar]
- Coen E. S., Thoday J. M., Dover G. Rate of turnover of structural variants in the rDNA gene family of Drosophila melanogaster. Nature. 1982 Feb 18;295(5850):564–568. doi: 10.1038/295564a0. [DOI] [PubMed] [Google Scholar]
- Dawid I. B., Wellauer P. K., Long E. O. Ribosomal DNA in Drosophila melanogaster. I. Isolation and characterization of cloned fragments. J Mol Biol. 1978 Dec 25;126(4):749–768. doi: 10.1016/0022-2836(78)90018-9. [DOI] [PubMed] [Google Scholar]
- Endow S. A., Komma D. J., Atwood K. C. Ring chromosomes and rDNA magnification in Drosophila. Genetics. 1984 Dec;108(4):969–983. doi: 10.1093/genetics/108.4.969. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Endow S. A., Komma D. J. One-step and stepwise magnification of a bobbed lethal chromosome in Drosophila melanogaster. Genetics. 1986 Oct;114(2):511–523. doi: 10.1093/genetics/114.2.511. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Frankham R., Briscoe D. A., Nurthen R. K. Unequal crossing over at the rRNA tandon as a source of quantitative genetic variation in Drosophila. Genetics. 1980 Jul;95(3):727–742. doi: 10.1093/genetics/95.3.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gandhi V. V., Sharp Z. D., Procunier J. D. Analysis of Y chromosome nucleolar organizer mutants in Drosophila melanogaster. Biochem Biophys Res Commun. 1982 Jan 29;104(2):778–784. doi: 10.1016/0006-291x(82)90705-7. [DOI] [PubMed] [Google Scholar]
- Gillings M. R., Frankham R., Speirs J., Whalley M. X-Y Exchange and the Coevolution of the X and Y Rdna Arrays in Drosophila melanogaster. Genetics. 1987 Jun;116(2):241–251. doi: 10.1093/genetics/116.2.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Glover D. M., Hogness D. S. A novel arrangement of the 18S and 28S sequences in a repeating unit of Drosophila melanogaster rDNA. Cell. 1977 Feb;10(2):167–176. doi: 10.1016/0092-8674(77)90212-4. [DOI] [PubMed] [Google Scholar]
- Hardy R. W., Lindsley D. L., Livak K. J., Lewis B., Siversten A. L., Joslyn G. L., Edwards J., Bonaccorsi S. Cytogenetic analysis of a segment of the Y chromosome of Drosophila melanogaster. Genetics. 1984 Aug;107(4):591–610. doi: 10.1093/genetics/107.4.591. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kalumuck K. E., Procunier J. D. Nonselective amplification of ribosomal DNA repeat units in compensating genotypes of Drosophila melanogaster. Biochem Genet. 1984 Jun;22(5-6):453–465. doi: 10.1007/BF00484516. [DOI] [PubMed] [Google Scholar]
- Kalumuck K. E., Procunier J. D. Suppression of ribosomal RNA genes in Drosophila melanogaster. Genet Res. 1984 Dec;44(3):351–357. doi: 10.1017/s0016672300026586. [DOI] [PubMed] [Google Scholar]
- Kidd S. J., Glover D. M. Drosophila melanogaster ribosomal DNA containing type II insertions is variably transcribed in different strains and tissues. J Mol Biol. 1981 Oct 5;151(4):645–662. doi: 10.1016/0022-2836(81)90428-9. [DOI] [PubMed] [Google Scholar]
- Komma D. J., Endow S. A. Incomplete Y chromosomes promote magnification in male and female Drosophila. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2382–2386. doi: 10.1073/pnas.84.8.2382. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Komma D. J., Endow S. A. Magnification of the ribosomal genes in female Drosophila melanogaster. Genetics. 1986 Nov;114(3):859–874. doi: 10.1093/genetics/114.3.859. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Livak K. J. Organization and mapping of a sequence on the Drosophila melanogaster X and Y chromosomes that is transcribed during spermatogenesis. Genetics. 1984 Aug;107(4):611–634. doi: 10.1093/genetics/107.4.611. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Long E. O., Collins M., Kiefer B. I., Dawid I. B. Expression of the ribosomal DNA insertions in bobbed mutants of Drosophila melanogaster. Mol Gen Genet. 1981;182(3):377–384. doi: 10.1007/BF00293925. [DOI] [PubMed] [Google Scholar]
- Long E. O., Dawid I. B. Repeated genes in eukaryotes. Annu Rev Biochem. 1980;49:727–764. doi: 10.1146/annurev.bi.49.070180.003455. [DOI] [PubMed] [Google Scholar]
- Maddern R. H. Exchange between the ribosomal RNA genes of X and Y chromosomes in Drosophila melanogaster males. Genet Res. 1981 Aug;38(1):1–7. doi: 10.1017/s001667230002036x. [DOI] [PubMed] [Google Scholar]
- McKee B., Lindsley D. L. Inseparability of X-Heterochromatic Functions Responsible for X:Y Pairing, Meiotic Drive, and Male Fertility in Drosophila melanogaster. Genetics. 1987 Jul;116(3):399–407. doi: 10.1093/genetics/116.3.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miller J. R., Hayward D. C., Glover D. M. Transcription of the 'non-transcribed' spacer of Drosophila melanogaster rDNA. Nucleic Acids Res. 1983 Jan 11;11(1):11–19. doi: 10.1093/nar/11.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ohta T., Dover G. A. Population genetics of multigene families that are dispersed into two or more chromosomes. Proc Natl Acad Sci U S A. 1983 Jul;80(13):4079–4083. doi: 10.1073/pnas.80.13.4079. [DOI] [PMC free article] [PubMed] [Google Scholar]
- RITOSSA F. M., SPIEGELMAN S. LOCALIZATION OF DNA COMPLEMENTARY TO RIBOSOMAL RNA IN THE NUCLEOLUS ORGANIZER REGION OF DROSOPHILA MELANOGASTER. Proc Natl Acad Sci U S A. 1965 Apr;53:737–745. doi: 10.1073/pnas.53.4.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
- Ritossa F. M., Scala G. Equilibrium variations in the redundancy of rDNA in Drosophila melanogaster. Genetics. 1969;61(1 Suppl):305–317. [PubMed] [Google Scholar]
- Ritossa F. Procedure for magnification of lethal deletions of genes for ribosomal RNA. Nat New Biol. 1972 Nov 22;240(99):109–111. doi: 10.1038/newbio240109a0. [DOI] [PubMed] [Google Scholar]
- Rogers S. O., Bendich A. J. Heritability and Variability in Ribosomal RNA Genes of Vicia faba. Genetics. 1987 Oct;117(2):285–295. doi: 10.1093/genetics/117.2.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roiha H., Miller J. R., Woods L. C., Glover D. M. Arrangements and rearrangements of sequences flanking the two types of rDNA insertion in D. melanogaster. Nature. 1981 Apr 30;290(5809):749–753. doi: 10.1038/290749a0. [DOI] [PubMed] [Google Scholar]
- Tartof K. D. Evolution of transcribed and spacer sequences in the ribosomal RNA genes of Drosophila. Cell. 1979 Jul;17(3):607–614. doi: 10.1016/0092-8674(79)90268-x. [DOI] [PubMed] [Google Scholar]
- Tartof K. D. Increasing the multiplicity of ribosomal RNA genes in Drosophila melanogaster. Science. 1971 Jan 22;171(3968):294–297. doi: 10.1126/science.171.3968.294. [DOI] [PubMed] [Google Scholar]
- Tautz D., Hancock J. M., Webb D. A., Tautz C., Dover G. A. Complete sequences of the rRNA genes of Drosophila melanogaster. Mol Biol Evol. 1988 Jul;5(4):366–376. doi: 10.1093/oxfordjournals.molbev.a040500. [DOI] [PubMed] [Google Scholar]
- Terracol R., Prud'homme N. Differential elimination of rDNA genes in bobbed mutants of Drosophila melanogaster. Mol Cell Biol. 1986 Apr;6(4):1023–1031. doi: 10.1128/mcb.6.4.1023. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wellauer P. K., Dawid I. B., Tartof K. D. X and Y chromosomal ribosomal DNA of Drosophila: comparison of spacers and insertions. Cell. 1978 Jun;14(2):269–278. doi: 10.1016/0092-8674(78)90113-7. [DOI] [PubMed] [Google Scholar]
- Williams S. M., Furnier G. R., Fuog E., Strobeck C. Evolution of the ribosomal DNA spacers of Drosophila melanogaster: different patterns of variation on X and Y chromosomes. Genetics. 1987 Jun;116(2):225–232. doi: 10.1093/genetics/116.2.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Williams S. M., Strobeck C. Sister chromatid exchange and the evolution of rDNA spacer length. J Theor Biol. 1985 Oct 21;116(4):625–636. doi: 10.1016/s0022-5193(85)80092-8. [DOI] [PubMed] [Google Scholar]
- Yagura T., Yagura M., Muramatsu M. Drosophila melanogaster has different ribosomal RNA sequences on S and Y chromosomes. J Mol Biol. 1979 Oct 9;133(4):533–547. doi: 10.1016/0022-2836(79)90406-6. [DOI] [PubMed] [Google Scholar]
- de Cicco D. V., Glover D. M. Amplification of rDNA and type I sequences in Drosophila males deficient in rDNA. Cell. 1983 Apr;32(4):1217–1225. doi: 10.1016/0092-8674(83)90304-5. [DOI] [PubMed] [Google Scholar]