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The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. III. Element abundances in heterochromatin

Published online by Cambridge University Press:  14 April 2009

Brian Charlesworth*
Affiliation:
Department of Ecology and Evolution, The University of Chicago, 1101 E. 57th St, Chicago IL 60637-1573, USA
Philippe Jarne
Affiliation:
Department of Ecology and Evolution, The University of Chicago, 1101 E. 57th St, Chicago IL 60637-1573, USA
Stavroula Assimacopoulos
Affiliation:
Department of Ecology and Evolution, The University of Chicago, 1101 E. 57th St, Chicago IL 60637-1573, USA
*
* Corresponding author.
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The total genomic copy numbers of ten families of transposable elements of Drosophila melanogaster in a set of ten isogenic lines derived from a natural population were estimated by slot-blotting. The numbers of euchromatic copies of members of each family were determined for each line by in situ hybridization of element probes to polytene chromosomes. Heterochromatic numbers were estimated by subtraction of the euchromatic counts from the total numbers. There was considerable variation between element families and lines in heterochromatic abundances, and the variance between lines for many elements was much greater for the heterochromatin than for the euchromatin. The data are consistent with the view that much of the β-heterochromatin consists of sequences derived from transposable elements. They are also consistent with the hypothesis that similar evolutionary forces control element abundances in both the euchromatin and heterochromatin, although amplification of inert sequences derived from transposable elements may be in part responsible for their accumulation in heterochromatin.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1994

References

Ananiev, E. V., Barsky, V. E., Ilyin, Y. V. & Rysic, M. V. (1984). The arrangement of transposable elements in the polytene chromosomes of Drosophila melanogaster. Chromosoma 90, 366377.CrossRefGoogle Scholar
Ashburner, M. (1989). Drosophila. A Laboratory Handbook. Cold Spring Harbor N.Y.: Cold Spring Harbor Laboratory Press.Google Scholar
Brown, P. C, Tlsty, T. D. & Schimke, R. T. (1983). Enhancement of methotrexate resistance and dihydrofolate reductase gene amplification by treatment of mouse 3T6 cells with hydroxyurea. Molecular and Cellular Biology 3, 10971107.Google ScholarPubMed
Caizzi, R., Caggese, C. & Pimpinelli, S. (1993). Bari-1, a new transposon-like family in Drosophila melanogaster with a unique heterochromatic organization. Genetics 133, 335345.CrossRefGoogle ScholarPubMed
Carlson, M. & Brutlag, D. L. (1978). One of the copia genes is adjacent to satellite DNA in Drosophila melanogaster. Cell 15, 733742.CrossRefGoogle Scholar
Charlesworth, B. (1991). Transposable elements in natural populations with a mixture of selected and neutral insertion sites. Genetical Research 57, 127134.CrossRefGoogle ScholarPubMed
Charlesworth, B. & Charlesworth, D. (1985). Genetic variation in recombination in Drosophila. I. Responses to selection and preliminary genetic analysis. Heredity 54, 7184.CrossRefGoogle Scholar
Charlesworth, B. & Langley, C. H. (1989). The population genetics of Drosophila transposable elements. Annual Review of Genetics 23, 251287.CrossRefGoogle ScholarPubMed
Charlesworth, B. & Lapid, A. (1989). A study of ten transposable elements on X chromosomes from a population of Drosophila melanogaster. Genetical Research 54, 113125.CrossRefGoogle ScholarPubMed
Charlesworth, B., Lapid, A & Canada, D. (1992a). The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. I. Element frequencies and distribution. Genetical Research 60, 103114.CrossRefGoogle Scholar
Charlesworth, B., Lapid, A. & Canada, D. (1992b). The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. II. Inferences on the nature of selection against elements. Genetical Research 60, 115130.CrossRefGoogle Scholar
Charlesworth, B., Sniegowski, P. & Stephan, W. (1994). The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371, 215220.CrossRefGoogle ScholarPubMed
Danilevskaya, O., Lofsky, A., Kurenova, E. & Pardue, M. L. (1993). The Y chromosome of Drosophila melanogaster contains a distinctive subclass of HeT-A related repeats. Genetics 134, 531543.CrossRefGoogle Scholar
Devlin, R. H., Bingham, B. & Wakimoto, B. T. (1990). The organization and expression of the light gene, a heterochromatic gene of Drosophila. Genetics 125, 129140.CrossRefGoogle ScholarPubMed
Nocera, P. P. Di & Dawid, I. B. (1983). Interdigitated arrangement of two oligo(a)-terminated DNA sequences in Drosophila. Nucleic Acids Research 11, 54755482.CrossRefGoogle ScholarPubMed
Dunsmuir, P., Brorein, W. J., Simon, M. A. & Rubin, G. M. (1980). Insertion of the Drosophila transposable element copia generates a 5 base pair insertion. Cell 21, 575579.CrossRefGoogle Scholar
Eanes, W. F., Wesley, C. & Charlesworth, B. (1992). Accumulation of P elements in minority inversions in natural populations of Drosophila melanogaster. Genetical Research 59, 19.CrossRefGoogle ScholarPubMed
Engels, W. R. (1989). P elements in Drosophila. In Mobile DNA (ed. Berg, D. E. and Howe, M. M.), pp. 437484. Washington, D.D.: American Society of Microbiology.Google Scholar
Finnegan, D. J. & Fawcett, D. H. (1986). Transposable elements in Drosophila melanogaster. Oxford Surveys on Eukaryote Genes 3, 162.Google ScholarPubMed
Ganguly, R., Swanson, K. D., Ray, K. & Krishnan, R. (1992). A Bam Hl repeat element is predominantly associated with the degenerating neo-Y chromosome of Drosophila miranda but absent in D. melanogaster genome. Proceedings of the National Academy of Sciences of the USA 89, 13401344.CrossRefGoogle Scholar
Haigh, J. (1978). The accumulation of deleterious genes in a population. Theoretical Population Biology 14, 251267.CrossRefGoogle ScholarPubMed
Heitz, E. (1934). Über α und β-Heterochromatin sowie Konstanz und Bau der Chromomeren bei Drosophila. Biologisches Zentralblatt 54, 588609.Google Scholar
Hilliker, A. J., Appels, R. & Schalet, A. (1980). The genetic analysis of D. melanogaster heterochromatin. Cell 21, 607619.CrossRefGoogle ScholarPubMed
Hoel, P. G. (1962). Introduction to Mathematical Statistics. 3rd ed. New York: John Wiley.Google Scholar
Jowett, T. (1986). Preparation of nucleic acids. In Drosophila. A Practical Approach (ed. Roberts, D. B.), pp. 275286. Oxford: IRL Press.Google Scholar
Kidd, S. J. & Glover, D. M. (1980). A DNA segment from D. melanogaster which contains five tandemly repeating units homologous to the major rDNA insertion. Cell 19, 103119.CrossRefGoogle Scholar
Lakhotia, S. C. & Jacob, J. (1974). EM autoradiographic studies on polytene nuclei of Drosophila melanogaster. II. Organization and transcriptive activity of the chromocenter. Experimental Cell Research 86, 253263.CrossRefGoogle Scholar
Lefevre, G. (1976). A photographic representation of the polytene chromosomes of Drosophila melanogaster salivary glands. In The Genetics and Biology of Drosophila. Vol. 1a (ed. Ashburner, M. and Novitski, E.), pp. 3136. London: Academic Press.Google Scholar
Levis, R. W., Ganesan, R., Houtchens, K., Tolar, L. A. & Sheen, F. (1993). Transposons in place of telomeric repeats at a Drosophila telomere. Cell 75, 10831093.CrossRefGoogle Scholar
Lindsley, D. L. & Zimm, G. G. (1992). The Genome of Drosophila melanogaster. San Diego, CA: Academic Press.Google Scholar
Lohe, A. R. & Brutlag, D. L. (1986). Multiplicity of satellite DNA sequences in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the USA 83, 606700.CrossRefGoogle ScholarPubMed
Lohe, A. R. & Brutlag, D. L. (1987). Adjacent satellite DNA segments in Drosophila. Structure of junctions. Journal of Molecular Biology 194, 171179.CrossRefGoogle ScholarPubMed
Lohe, A. R., Hilliker, A. J. & Roberts, P. A. (1993). Mapping simple repeated sequences in heterochromatin of Drosophila melanogaster. Genetics 134, 11491174.CrossRefGoogle ScholarPubMed
Lyckegaard, E. M. S. & Clark, A. G. (1991). Evolution of ribosomal gene copy number of the sex chromosomes of Drosophila melanogaster. Molecular Biology and Evolution 8, 458474.Google ScholarPubMed
Miklos, G. L. G. (1985). Localized highly repetitive DNA sequences in vertebrate and invertebrate genomes. In Molecular Evolutionary Genetics (ed. Maclntyre, R. J.), pp. 240321. New York: Plenum Press.Google Scholar
Miklos, G. L. G. & Cotsell, J. N. (1990). Chromosome structure at interfaces between major chromatin types. BioEssays 12, 16.CrossRefGoogle ScholarPubMed
Miklos, G. L. G., Healy, M. J., Pain, P., Howells, A. J. & Russell, R. J. (1984). Molecular genetic studies on the euchromatin-heterochromatin junction in the X chromosome of Drosophila melanogaster. I. A cloned entry point near to the uncoordinated (unc) locus. Chromosoma 89, 218227.CrossRefGoogle Scholar
Miklos, G. L. G., Yamamoto, M.-T., Davies, J. & Pirrotta, V. (1988). Microcloning reveals a high, frequency of repetitive sequences characteristic of chromosome 4 and the β-heterochromatin of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the USA 85, 20512055.CrossRefGoogle ScholarPubMed
Montchamp-Moreau, C., Ronsseray, S., Jacques, M., Lehmann, M. & Anxholabehére, D. (1993). Distribution and conservation of sequences homologous to the 1731 retrotransposon in Drosophila. Molecular Biology and Evolution 10, 791803.Google Scholar
Montgomery, E. A., Charlesworth, B. & Langley, C. H. (1987). A test for the role of natural selection in the stabilization of transposable element copy number in a population of Drosophila. Genetical Research 49, 3141.CrossRefGoogle Scholar
Montgomery, E. A., Huang, S.-M., Langley, C. H. & Judd, B. H. (1991). Chromosome rearrangement by ectopic recombination in Drosophila melanogaster: genome structure and evolution. Genetics 129, 10851098.CrossRefGoogle ScholarPubMed
Nurminsky, D. I., Shevelyov, Y. Y., Nuzhdin, S. V. & Gvozdev, V. A. (1994). Structure, molecular evolution and maintenance of copy number of extended repeated structures in the X-heterochromatin of Drosophila melanogaster. Molecular and General Genetics 103, 277285.Google ScholarPubMed
Pimpinelli, S., Bonaccorsi, S., Gatti, M. & Sandier, L. (1986). The peculiar genetic organization of Drosophila heterochromatin. Trends in Genetics 2, 1720.CrossRefGoogle Scholar
Potter, S. S., Brorein, W. J., Dunsmuir, P. & Rubin, G. M. (1979). Transposition of elements of the 412, copia and 297 dispersed repeated gene families in Drosophila. Cell 17, 415427.CrossRefGoogle ScholarPubMed
Roiha, H., Miller, J. R., Woods, L. C. & Glover, D. M. (1981). Arrangements and rearrangements of sequences flanking the two types of rDNA insertion in Drosophila melanogaster. Nature 290, 749753.CrossRefGoogle Scholar
Sambrook, J., Maniatis, T. & Fritsch, E. F. (1989). Molecular Cloning. A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.Google Scholar
Schalet, A. & Lefevre, G. (1976). The proximal region of the X chromosome. In The Genetics and Biology of Drosophila. Vol. 1 b (ed. Ashburner, M. and Novitski, E.), pp. 847902. London: Academic Press.Google Scholar
Sniegowski, P. D. & Charlesworth, B. (1994). Transposable element numbers in cosmopolitan inversions from a natural population of Drosophila melanogaster. Genetics 137, 815827.CrossRefGoogle ScholarPubMed
Sniegowski, P. D., Pringle, A. & Hughes, K. A. (1994). Effect of autosomal inversions on meiotic exchange in distal and proximal regions of the X chromosome in a natural population of Drosophila melanogaster. Genetical Research 63, 5762.CrossRefGoogle Scholar
Spofford, J. B. (1976). Position-effect variegation in Drosophila. In The Genetics and Biology of Drosophila. Vol. 1c (ed. Ashburner, M. and Novitski, E.), pp. 9551019. London: Academic Press.Google Scholar
Steinemann, M. & Steinemann, S. (1992). Degenerating Y chromosome of Drosophila miranda: a trap for retrotransposons. Proceedings of the National Academy of Sciences of the USA 89, 75917595.CrossRefGoogle Scholar
Stephan, W., Chao, L. & Smale, J. G. (1993). The advance of Muller's ratchet in a haploid asexual population: approximate solutions based on diffusion theory. Genetical Research 61, 225232.CrossRefGoogle Scholar
Strobel, E., Dunsmuir, P. & Rubin, G. M. (1979). Polymorphism in the locations of elements of the 412, copia and 297 dispersed repeated gene families in Drosophila. Cell 17, 429439.CrossRefGoogle ScholarPubMed
Szauter, P. (1984). An analysis of regional constraints on crossing over in Drosophila melanogaster. Genetics 106, 4571.CrossRefGoogle ScholarPubMed
Valgeirsdottir, K., Traverse, K. L. & Pardue, M. L. (1990). HeT DNA: a family of mosaic repeated sequences specific for heterochromatin in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the USA 87, 77988002.CrossRefGoogle ScholarPubMed
Vaury, C, Bucheton, A. & Pelisson, A. (1989). The β-heterochromatin sequences flanking the I elements are themselves defective transposable elements. Chromosoma 98, 215224.CrossRefGoogle ScholarPubMed
Wieschaus, E. & Nusslein-Volhard, C. (1986). Looking at embryos. In Drosophila. A Practical Approach (ed. Roberts, D. B.), pp. 199228. Oxford: IRL Press.Google Scholar
Yamamoto, M.-T., Mitchelson, A., Tudor, M., O'Hare, K., Davies, J. A. & Miklos, G. L. G. (1990). Molecular and cytogenetic analysis of the heterochromatin-euchromatin junction region of the Drosophila melanogaster X chromosome. Genetics 125, 821832.CrossRefGoogle ScholarPubMed
Young, M. (1979). Middle repetitive DNA: a fluid component of the Drosophila genome. Proceedings of the National Academy of Sciences of the USA 76, 62746278.CrossRefGoogle ScholarPubMed