Abstract
Heterochromatin in Drosophila has unusual genetic, cytological and molecular properties. Highly repeated DNA sequences (satellites) are the principal component of heterochromatin. Using probes from cloned satellites, we have constructed a chromosome map of 10 highly repeated, simple DNA sequences in heterochromatin of mitotic chromosomes of Drosophila melanogaster. Despite extensive sequence homology among some satellites, chromosomal locations could be distinguished by stringent in situ hybridizations for each satellite. Only two of the localizations previously determined using gradient-purified bulk satellite probes are correct. Eight new satellite localizations are presented, providing a megabase-level chromosome map of one-quarter of the genome. Five major satellites each exhibit a multichromosome distribution, and five minor satellites hybridize to single sites on the Y chromosome. Satellites closely related in sequence are often located near one another on the same chromosome. About 80% of Y chromosome DNA is composed of nine simple repeated sequences, in particular (AAGAC)(n) (8 Mb), (AAGAG)(n) (7 Mb) and (AATAT)(n) (6 Mb). Similarly, more than 70% of the DNA in chromosome 2 heterochromatin is composed of five simple repeated sequences. We have also generated a high resolution map of satellites in chromosome 2 heterochromatin, using a series of translocation chromosomes whose breakpoints in heterochromatin were ordered by N-banding. Finally, staining and banding patterns of heterochromatic regions are correlated with the locations of specific repeated DNA sequences. The basis for the cytochemical heterogeneity in banding appears to depend exclusively on the different satellite DNAs present in heterochromatin.
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- Abad J. P., Carmena M., Baars S., Saunders R. D., Glover D. M., Ludeña P., Sentis C., Tyler-Smith C., Villasante A. Dodeca satellite: a conserved G+C-rich satellite from the centromeric heterochromatin of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1992 May 15;89(10):4663–4667. doi: 10.1073/pnas.89.10.4663. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ayles G. B., Sanders T. G., Kiefer B. I., Suzuki D. T. Temperature-sensitive mutations in Drosophila melanogaster. XI. Male sterile mutants of the Y chromosome. Dev Biol. 1973 Jun;32(2):239–257. doi: 10.1016/0012-1606(73)90239-x. [DOI] [PubMed] [Google Scholar]
- Barigozzi C., Dolfini S., Fraccaro M., Raimondi G. R., Tiepolo L. In vitro study of the DNA replication patterns of somatic chromosomes of Drosophila melanogaster. Exp Cell Res. 1966 Aug;43(1):231–234. doi: 10.1016/0014-4827(66)90399-5. [DOI] [PubMed] [Google Scholar]
- Bonaccorsi S., Lohe A. Fine mapping of satellite DNA sequences along the Y chromosome of Drosophila melanogaster: relationships between satellite sequences and fertility factors. Genetics. 1991 Sep;129(1):177–189. doi: 10.1093/genetics/129.1.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bridges C. B. Non-Disjunction as Proof of the Chromosome Theory of Heredity (Concluded). Genetics. 1916 Mar;1(2):107–163. doi: 10.1093/genetics/1.2.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brutlag D., Appels R., Dennis E. S., Peacock W. J. Highly repeated DNA in Drosophila melanogaster. J Mol Biol. 1977 May 5;112(1):31–47. doi: 10.1016/s0022-2836(77)80154-x. [DOI] [PubMed] [Google Scholar]
- Carlson M., Brutlag D. Different regions of a complex statellite DNA vary in size and sequence of the repeating unit. J Mol Biol. 1979 Dec 5;135(2):483–500. doi: 10.1016/0022-2836(79)90448-0. [DOI] [PubMed] [Google Scholar]
- Carlson M., Brutlag D. One of the copia genes is adjacent to satellite DNA in Drosophila melanogaster. Cell. 1978 Nov;15(3):733–742. doi: 10.1016/0092-8674(78)90259-3. [DOI] [PubMed] [Google Scholar]
- Danilevskaya O. N., Kurenova E. V., Pavlova M. N., Bebehov D. V., Link A. J., Koga A., Vellek A., Hartl D. L. He-T family DNA sequences in the Y chromosome of Drosophila melanogaster share homology with the X-linked stellate genes. Chromosoma. 1991 Feb;100(2):118–124. doi: 10.1007/BF00418245. [DOI] [PubMed] [Google Scholar]
- DiBartolomeis S. M., Tartof K. D., Jackson F. R. A superfamily of Drosophila satellite related (SR) DNA repeats restricted to the X chromosome euchromatin. Nucleic Acids Res. 1992 Mar 11;20(5):1113–1116. doi: 10.1093/nar/20.5.1113. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Endow S. A., Polan M. L., Gall J. G. Satellite DNA sequences of Drosophila melanogaster. J Mol Biol. 1975 Aug 25;96(4):665–692. doi: 10.1016/0022-2836(75)90145-x. [DOI] [PubMed] [Google Scholar]
- Fry K., Brutlag D. Detection and resolution of closely related satellite DNA sequences by molecular cloning. J Mol Biol. 1979 Dec 15;135(3):581–593. doi: 10.1016/0022-2836(79)90165-7. [DOI] [PubMed] [Google Scholar]
- Gall J. G., Cohen E. H., Polan M. L. Reptitive DNA sequences in drosophila. Chromosoma. 1971;33(3):319–344. doi: 10.1007/BF00284948. [DOI] [PubMed] [Google Scholar]
- Goldstein L. S., Hardy R. W., Lindsley D. L. Structural genes on the Y chromosome of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7405–7409. doi: 10.1073/pnas.79.23.7405. [DOI] [PMC free article] [PubMed] [Google Scholar]
- HANNAH A. Localization and function of heterochromatin in Drosophila melanogaster. Adv Genet. 1951;4:87–125. doi: 10.1016/s0065-2660(08)60232-1. [DOI] [PubMed] [Google Scholar]
- Hartl D. L., Ajioka J. W., Cai H., Lohe A. R., Lozovskaya E. R., Smoller D. A., Duncan I. W. Towards a Drosophila genome map. Trends Genet. 1992 Feb;8(2):70–75. doi: 10.1016/0168-9525(92)90353-6. [DOI] [PubMed] [Google Scholar]
- Hilliker A. J., Appels R. Pleiotropic effects associated with the deletion of heterochromatin surrounding rDNA on the X chromosome of Drosophila. Chromosoma. 1982;86(4):469–490. doi: 10.1007/BF00330122. [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]
- Hilliker A. J. Genetic analysis of the centromeric heterochromatin of chromosome 2 of Drosophila melanogaster: deficiency mapping of EMS-induced lethal complementation groups. Genetics. 1976 Aug;83(4):765–782. doi: 10.1093/genetics/83.4.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hilliker A. J., Trusis-Coulter S. N. Analysis of the functional significance of linkage group conservation in Drosophila. Genetics. 1987 Oct;117(2):233–244. doi: 10.1093/genetics/117.2.233. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hsieh T., Brutlag D. Sequence and sequence variation within the 1.688 g/cm3 satellite DNA of Drosophila melanogaster. J Mol Biol. 1979 Dec 5;135(2):465–481. doi: 10.1016/0022-2836(79)90447-9. [DOI] [PubMed] [Google Scholar]
- Inouye S., Yuki S., Saigo K. Complete nucleotide sequence and genome organization of a Drosophila transposable genetic element, 297. Eur J Biochem. 1986 Jan 15;154(2):417–425. doi: 10.1111/j.1432-1033.1986.tb09414.x. [DOI] [PubMed] [Google Scholar]
- Langer P. R., Waldrop A. A., Ward D. C. Enzymatic synthesis of biotin-labeled polynucleotides: novel nucleic acid affinity probes. Proc Natl Acad Sci U S A. 1981 Nov;78(11):6633–6637. doi: 10.1073/pnas.78.11.6633. [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]
- Lohe A. R., Brutlag D. L. Adjacent satellite DNA segments in Drosophila structure of junctions. J Mol Biol. 1987 Mar 20;194(2):171–179. doi: 10.1016/0022-2836(87)90366-4. [DOI] [PubMed] [Google Scholar]
- Lohe A. R., Brutlag D. L. Identical satellite DNA sequences in sibling species of Drosophila. J Mol Biol. 1987 Mar 20;194(2):161–170. doi: 10.1016/0022-2836(87)90365-2. [DOI] [PubMed] [Google Scholar]
- Lohe A. R., Brutlag D. L. Multiplicity of satellite DNA sequences in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1986 Feb;83(3):696–700. doi: 10.1073/pnas.83.3.696. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lohe A. R., Roberts P. A. An unusual Y chromosome of Drosophila simulans carrying amplified rDNA spacer without rRNA genes. Genetics. 1990 Jun;125(2):399–406. doi: 10.1093/genetics/125.2.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marchant G. E., Holm D. G. Genetic Analysis of the Heterochromatin of Chromosome 3 in Drosophila Melanogaster. II. Vital Loci Identified through Ems Mutagenesis. Genetics. 1988 Oct;120(2):519–532. doi: 10.1093/genetics/120.2.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marchant G. E., Holm D. G. Genetic analysis of the heterochromatin of chromosome 3 in Drosophila melanogaster. I. Products of compound-autosome detachment. Genetics. 1988 Oct;120(2):503–517. doi: 10.1093/genetics/120.2.503. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Muller H. J., Gershenson S. M. Inert Regions of Chromosomes as the Temporary Products of Individual Genes. Proc Natl Acad Sci U S A. 1935 Feb;21(2):69–75. doi: 10.1073/pnas.21.2.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Peacock W. J., Brutlag D., Goldring E., Appels R., Hinton C. W., Lindsley D. L. The organization of highly repeated DNA sequences in Drosophila melanogaster chromosomes. Cold Spring Harb Symp Quant Biol. 1974;38:405–416. doi: 10.1101/sqb.1974.038.01.043. [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]
- Pimpinelli S., Dimitri P. Cytogenetic analysis of segregation distortion in Drosophila melanogaster: the cytological organization of the Responder (Rsp) locus. Genetics. 1989 Apr;121(4):765–772. doi: 10.1093/genetics/121.4.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pimpinelli S., Santini G., Gatti M. Characterization of Drosophila heterochromatin. II. C- and N-banding. Chromosoma. 1976 Sep 24;57(4):377–386. doi: 10.1007/BF00332161. [DOI] [PubMed] [Google Scholar]
- Pimpinelli S., Sullivan W., Prout M., Sandler L. On biological functions mapping to the heterochromatin of Drosophila melanogaster. Genetics. 1985 Apr;109(4):701–724. doi: 10.1093/genetics/109.4.701. [DOI] [PMC free article] [PubMed] [Google Scholar]
- ROBERTS P. A. DIFFERENCE IN THE BEHAVIOR OF EU- AND HETERO-CHROMATIN: CROSSING-OVER. Nature. 1965 Feb 13;205:725–726. doi: 10.1038/205725b0. [DOI] [PubMed] [Google Scholar]
- Rudkin G. T. Non replicating DNA in Drosophila. Genetics. 1969;61(1 Suppl):227–238. [PubMed] [Google Scholar]
- Spear B. B. The genes for ribosomal RNA in diploid and polytene chromosomes of Drosophila melanogaster. Chromosoma. 1974;48(2):159–179. doi: 10.1007/BF00283961. [DOI] [PubMed] [Google Scholar]
- Spradling A. C., de Cicco D. V., Wakimoto B. T., Levine J. F., Kalfayan L. J., Cooley L. Amplification of the X-linked Drosophila chorion gene cluster requires a region upstream from the s38 chorion gene. EMBO J. 1987 Apr;6(4):1045–1053. doi: 10.1002/j.1460-2075.1987.tb04857.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Steffensen D. M., Appels R., Peacock W. J. The distribution of two highly repeated DNA sequences within Drosophila melanogaster chromosomes. Chromosoma. 1981;82(4):525–541. doi: 10.1007/BF00295011. [DOI] [PubMed] [Google Scholar]
- Szabo P., Elder R., Steffensen D. M., Uhlenbeck O. C. Quantitative in situ hybridization of ribosomal RNA species to polytene chromosomes of Drosophila melanogaster. J Mol Biol. 1977 Sep 25;115(3):539–563. doi: 10.1016/0022-2836(77)90170-x. [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]
- Williamson J. H. Allelic complementation between mutants in the fertility factyors of the Y chromosome in Drosophila melanogaster. Mol Gen Genet. 1972;119(1):43–47. doi: 10.1007/BF00270442. [DOI] [PubMed] [Google Scholar]
- Williamson J. H. Ethyl methanesulfonate-induced mutants in the Y chromosome of Drosophila melanogaster. Mutat Res. 1970 Dec;10(6):597–605. doi: 10.1016/0027-5107(70)90087-4. [DOI] [PubMed] [Google Scholar]
- Wu C. I., Lyttle T. W., Wu M. L., Lin G. F. Association between a satellite DNA sequence and the Responder of Segregation Distorter in D. melanogaster. Cell. 1988 Jul 15;54(2):179–189. doi: 10.1016/0092-8674(88)90550-8. [DOI] [PubMed] [Google Scholar]