Abstract
The nucleolus organizers on the X and Y chromosomes of Drosophila melanogaster are the sites of 200-250 tandemly repeated genes for ribosomal RNA. As there is no meiotic crossing over in male Drosophila, the X and Y chromosomal rDNA arrays should be evolutionarily independent, and therefore divergent. The rRNAs produced by X and Y are, however, very similar, if not identical. Molecular, genetic and cytological analyses of a series of X chromosome rDNA deletions (bb alleles) showed that they arose by unequal exchange through the nucleolus organizers of the X and Y chromosomes. Three separate exchange events generated compound X·Y L chromosomes carrying mainly Y-specific rDNA. This led to the hypothesis that X-Y exchange is responsible for the coevolution of X and Y chromosomal rDNA. We have tested and confirmed several of the predictions of this hypothesis: First, X· YL chromosomes must be found in wild populations. We have found such a chromosome. Second, the X·YL chromosome must lose the YL arm, and/or be at a selective disadvantage to normal X+ chromosomes, to retain the normal morphology of the X chromosome. Six of seventeen sublines founded from homozygous X·YLbb stocks have become fixed for chromosomes with spontaneous loss of part or all of the appended YL. Third, rDNA variants on the X chromosome are expected to be clustered within the X+ nucleolus organizer, recently donated (" Y") forms being proximal, and X-specific forms distal. We present evidence for clustering of rRNA genes containing Type 1 insertions. Consequently, X-Y exchange is probably responsible for the coevolution of X and Y rDNA arrays.
Full Text
The Full Text of this article is available as a PDF (3.4 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Durica D. S., Krider H. M. Studies on the Ribosomal RNA Cistrons in Interspecific Drosophila Hybrids. II. Heterochromatic Regions Mediating Nucleolar Dominance. Genetics. 1978 May;89(1):37–64. doi: 10.1093/genetics/89.1.37. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Frankham R., Briscoe D. A., Nurthen R. K. Unequal crossing over at the rRNA locus as a source of quantitative genetic variation. Nature. 1978 Mar 2;272(5648):80–81. doi: 10.1038/272080a0. [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]
- Hawley R. S., Tartof K. D. The ribosomal DNA of Drosophila melanogaster is organized differently from that of Drosophila hydei. J Mol Biol. 1983 Jan 25;163(3):499–503. doi: 10.1016/0022-2836(83)90071-2. [DOI] [PubMed] [Google Scholar]
- Hilliker A. J., Appels R., Schalet A. The genetic analysis of D. melanogaster heterochromatin. Cell. 1980 Oct;21(3):607–619. doi: 10.1016/0092-8674(80)90424-9. [DOI] [PubMed] [Google Scholar]
- Indik Z. K., Tartof K. D. Long spacers among ribosomal genes of Drosophila melanogaster. Nature. 1980 Apr 3;284(5755):477–479. doi: 10.1038/284477a0. [DOI] [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. Expression of ribosomal DNA insertions in Drosophila melanogaster. Cell. 1979 Dec;18(4):1185–1196. doi: 10.1016/0092-8674(79)90231-9. [DOI] [PubMed] [Google Scholar]
- Maden B. E., Tartof K. Nature of the ribosomal RNA transcribed from the X and Y chromosomes of Drosophila melanogaster. J Mol Biol. 1974 Nov 25;90(1):51–64. doi: 10.1016/0022-2836(74)90255-1. [DOI] [PubMed] [Google Scholar]
- Miklos G. L., Gill A. C. Nucleotide sequences of highly repeated DNAs; compilation and comments. Genet Res. 1982 Feb;39(1):1–30. doi: 10.1017/s0016672300020711. [DOI] [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]
- Peacock W. J., Appels R., Endow S., Glover D. Chromosomal distribution of the major insert in Drosophila melanogaster 28S rRNA genes. Genet Res. 1981 Apr;37(2):209–214. doi: 10.1017/s0016672300020176. [DOI] [PubMed] [Google Scholar]
- Peacock W. J., Lohe A. R., Gerlach W. L., Dunsmuir P., Dennis E. S., Appels R. Fine structure and evolution of DNA in heterochromatin. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):1121–1135. doi: 10.1101/sqb.1978.042.01.113. [DOI] [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]
- Reeder R. H., Roan J. G. The mechanism of nucleolar dominance in Xenopus hybrids. Cell. 1984 Aug;38(1):38–44. doi: 10.1016/0092-8674(84)90524-5. [DOI] [PubMed] [Google Scholar]
- Renkawitz-Pohl R., Glätzer K. H., Kunz W. Ribosomal RNA genes with an intervening sequence are clustered within the X chromosomal ribosomal DNA of Drosophila hydei. J Mol Biol. 1981 May 5;148(1):95–101. doi: 10.1016/0022-2836(81)90237-0. [DOI] [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]
- Roiha H., Glover D. M. Chracterisation of complete type II insertions in cloned segments of ribosomal DNA from Drosophila melanogaster. J Mol Biol. 1980 Jun 25;140(2):341–355. doi: 10.1016/0022-2836(80)90110-2. [DOI] [PubMed] [Google Scholar]
- Roiha H., Read C. A., Browne M. J., Glover D. M. Widely differing degrees of sequence conservation of the two types of rDNA insertion within the melanogaster species sub-group of Drosophila. EMBO J. 1983;2(5):721–726. doi: 10.1002/j.1460-2075.1983.tb01491.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
- Tartof K. D. Redundant genes. Annu Rev Genet. 1975;9:355–385. doi: 10.1146/annurev.ge.09.120175.002035. [DOI] [PubMed] [Google Scholar]
- Tautz D., Renz M. An optimized freeze-squeeze method for the recovery of DNA fragments from agarose gels. Anal Biochem. 1983 Jul 1;132(1):14–19. doi: 10.1016/0003-2697(83)90419-0. [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]