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A 1·5 kb direct repeat sequence flanks the suppressor of forked gene at the euchromatin–heterochromatin boundary of the Drosophila melanogaster X chromosome

Published online by Cambridge University Press:  14 April 2009

Mark Tudor
Affiliation:
Department of Biochemistry, Imperial College of Science, Technology & Medicine, LondonSW7 2AZUK
Andrew Mitchelson
Affiliation:
Department of Biochemistry, Imperial College of Science, Technology & Medicine, LondonSW7 2AZUK
Kevin O'hare*
Affiliation:
Department of Biochemistry, Imperial College of Science, Technology & Medicine, LondonSW7 2AZUK
*
* Corresponding author. Fax: +44(171) 225 0960. e-mail: [email protected].
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A 1·5 kilobasepair repeated DNA sequence is duplicated in direct orientation so as to flank the suppressor of forked gene in the euchromatin–heterochromatin transition region on the X chromosome of Drosophila melanogaster. These two copies are almost identical, but DNA blotting, analysis of cloned sequences and database searches show that elsewhere in the genome, homologous sequences are poorly conserved. They are often associated with other repeats, suggesting that they may belong to a scrambled and clustered middle repetitive DNA family. The sequences do not appear to be related to transposable elements and their location in different strains is conserved. In situ hybridization to metaphase chromosomes shows that homologous sequences are concentrated in the pericentric regions of the autosomes and the X chromosome. The sequences are not significantly under-represented in DNA from polytene tissue and must lie in the replicated regions of polytene chromosomes. The almost perfect conservation of the two repeats around suppressor of forked in D. melanogaster suggests they arose by duplication or gene conversion. Suppression of recombination in this chromosomal region presumably allows this unusual organization to be stably maintained. In the X-ray induced allele, suppressor of forked-L26, the sequence between the repeats, including the gene, and one copy of the repeat have been deleted.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1996

References

Abad, J., Carmena, M., Baars, S., Saunders, R., Glover, D., Ludena, P., Sentis, C., Tyler-Smith, C., & Villasante, A., (1992). Dodeca satellite: a conserved G + C-rich satellite from the centromeric heterochromatin of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the USA 89, 46634667.Google Scholar
Carmena, M., & Gonzalez, C., (1995). Transposable elements map in a conserved pattern of distribution extending from beta-heterochromatin to centromeres in Drosophila melanogaster. Chromosoma 103, 676684.Google Scholar
Devlin, R. H., Bingham, B., & Wakimoto, B. T., (1990). The organization and expression of the light gene, a heterochromatic gene of Drosophila melanogaster. Genetics 125, 129140.CrossRefGoogle ScholarPubMed
Gall, J. G., (1973). Repetitive DNA in Drosophila. In Molecular Cytogenetics (ed. Hamkalo, B. A. & Papaconstantinou, J.), pp. 5974. New York: Plenum Press.Google Scholar
Galloni, M., Gyurkovics, H., Schedl, P., & Karch, F., (1993). The bluetail transposon: evidence for independent cis-regulatory domains and domain boundaries in the bithorax complex. EMBO Journal 12, 10871097.CrossRefGoogle ScholarPubMed
Gasser, S. M., & Laemmli, U. K., (1986). The organisation of chromatin loops—characterisation of a scaffold attachment site. EMBO Journal 5, 511518.CrossRefGoogle ScholarPubMed
Gatti, M., & Pimpinelli, S., (1992). Functional elements in Drosophila melanogaster heterochromatin. Annual Review of Genetics 26, 239275.Google Scholar
Glover, D., (1981). The rDNA of Drosophila melanogaster. Cell 26, 297298.Google Scholar
Healy, M., Russell, R., & Miklos, G., (1988). Molecular studies on interspersed repetitive and unique sequences in the region of the complementation group uncoordinated on the X chromosome of Drosophila melanogaster. Molecular and General Genetics 213, 6371.Google Scholar
Heitz, E., (1934). Über α- und β-Heterochromatin sowie Konstanz und Bau der Chromomeren bei Drosophila. Biologisches Zentralblatt 54, 588609.Google Scholar
Hoheisel, J. D., Lennon, G. G., Zehnetner, G., & Lehrach, H., (1991). Use of high coverage reference libraries of Drosophila melanogaster for relational data analysis: a step towards mapping and sequencing of the genome. Journal of Molecular Biology 220, 903914.CrossRefGoogle ScholarPubMed
Kellum, R., & Schedl, P., (1991). A position-effect assay for boundaries of higher order chromosomal domains. Cell 64, 941950.Google Scholar
Kellum, R., & Schedl, P., (1992). A group of SCS elements function as domain boundaries in an enhancer blocking assay. Molecular and Cellular Biology 12, 24242431.Google Scholar
Lamb, M. M., & Laird, C. D., (1987). Three euchromatic DNA sequences under-replicated in polytene chromosomes of Drosophila are localized in constrictions and ectopic fibers. Chromosoma 95, 227235.CrossRefGoogle ScholarPubMed
Langley, C, MacDonald, J., Miyashita, N., & Aguade, M., (1993). Lack of correlation between interspecific divergence and intraspecific polymorphism at the suppressor of forked region in Drosophila melanogaster and Drosophila simulans. Proceedings of the National Academy of Sciences of the USA 90, 18001803.CrossRefGoogle ScholarPubMed
Le, M. -H., Duricka, D., & Karpen, G. H., (1995). Islands of complex DNA are widespread in Drosophila centric heterochromatin. Genetics 141, 283303.CrossRefGoogle ScholarPubMed
Lefevre, G., (1981). The distribution of randomly recovered X-ray induced sex-linked genetic effects in Drosophila melanogaster. Genetics 99, 461480.Google Scholar
Lim, J. K., & Simmons, M. J., (1994). Gross chromosome rearrangements mediated by transposable elements in Drosophila melanogaster. BioEssays 16, 269275.CrossRefGoogle ScholarPubMed
Lindsley, D. L., & Zimm, G. G., (1992). The Genome of Drosophila melanogaster. New York: Academic Press.Google Scholar
Madueno, E., Papagiannakis, G., Rimmington, G., Saunders, R. D. C., Savakis, C, Sidén-Kiamos, I., Skavdis, G., Spanos, L., Trenear, J., Adam, P., Ashburner, M., Benos, P., Bolshakov, V. N., Coulson, D., Glover, D. M., Hermann, S., Kafatos, F. C., Louis, C, Majerus, T., & Modolell, J., (1995). A physical map of the X chromosome of Drosophila melanogaster: cosmid contigs and sequence tagged sites. Genetics 139, 16311647.CrossRefGoogle ScholarPubMed
Miklos, G. L. G., & Cotsell, J. N., (1990). Chromosome structure at interfaces between major chromatin types: α- and β-heterochromatin. BioEssays 12, 16.Google Scholar
Miklos, G. L. G., Healy, M. J., Pain, P., Howells, A. J., & Russell, R. J., (1984). Molecular and genetic studies on the euchromatin—heterochromatin transition region of the X chromosome of Drosophila melanogaster: 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.Google Scholar
Mitchelson, A., Simonelig, M., Williams, C., & O'Hare, K., (1993). Homology with Saccharomyces cerevisiae RNA 14 suggests that phenotype suppression in Drosophila melanogaster by suppressor of forked occurs at the level of RNA stability. Genes and Development 1, 241249.Google Scholar
Pardue, M. L., & Hennig, W., (1992). Heterochromatin: junk or collector's item? Chromosoma 100, 37.Google Scholar
Peacock, W., Lohe, A., Gerlach, W., Dunsmuir, P., Dennis, E., & Appels, R., (1978). Fine structure and evolution of DNA in heterochromatin. Cold Spring Harbor Symposia on Quantitative Biology 42, 11211135.CrossRefGoogle ScholarPubMed
Pimpinelli, S., Berloco, M., Fanti, L., Dimitri, P., Bonaccorsi, S., Marchetti, E., Caizzi, R., Caggese, C., & Gatti, M., (1995). Transposable elements are stable structural components of Drosophila melanogaster heterochromatin. Proceedings of the National Academy of Sciences of the USA 92, 38043808.Google Scholar
Roseman, R., Pirrotta, V., & Geyer, P. K., (1993). The su(Hw) protein insulates expression of the Drosophila melanogaster white gene from chromosomal position effects. EMBO Journal 12, 435442.CrossRefGoogle Scholar
Russell, R. J., Healy, M. J., & Oakeshott, J. G., (1992). Molecular analysis of the lethal (1) B214 region at the base of the X chromosome of Drosophila melanogaster. Chromosoma 101, 456466.Google Scholar
Schalet, A., & Lefevre, G., (1976). The proximal region of the X chromosome. In The Genetics and Biology of Drosophila, vol. 1b (ed. Ashburner, M. A. & Novitski, E.), pp. 848902. New York: Academic Press.Google Scholar
Segarra, C., & Aguade, M., (1992). Molecular organisation of the X chromosome in different species of the obscura group of Drosophila. Genetics 130, 513521.CrossRefGoogle ScholarPubMed
Simonelig, M., Elliott, K., Mitchelson, A., & O'Hare, K.(1996). Interallelic complementation at the suppressor of forked locus of Drosophila reveals complementation between suppressor of forked proteins mutated in different regions. Genetics 142, 12251235.Google Scholar
Spradling, A. C., Karpen, G., Glaser, R., & Zhang, P., (1993). DNA elimination in Drosophila. In Evolutionary Conservation of Developmental Mechanisms, pp. 3953. New York: Wiley-Liss.Google Scholar
Spradling, A. C., & Orr-Weaver, T., (1987). Regulation of DNA replication during Drosophila development. Annual Review of Genetics 21, 373403.CrossRefGoogle ScholarPubMed
Tartof, K. D., Hobbs, C., & Jones, M., (1984). A structural basis for variegating position effects. Cell 37, 869878.Google Scholar
Vaury, C, Abad, P., Pelisson, A., Lenoir, A., & Bucheton, A., (1990). Molecular characteristics of the heterochromatic I elements from a reactive strain of Drosophila melanogaster. Journal of Molecular Evolution 31, 424431.Google Scholar
Verma, R. S., (1988). Heterochromatin: Molecular and Structural Aspects. Cambridge: Cambridge University Press.Google Scholar
Williams, C. J., & O'Hare, K., (1996). Elimination of introns at the Drosophila suppressor of forked locus by P element mediated gene conversion shows that an RNA lacking a stop codon is dispensable. Genetics 143, 345351.CrossRefGoogle ScholarPubMed
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 using cloned DNA. Genetics 125, 821832.CrossRefGoogle ScholarPubMed
Young, M. W., (1979). Middle repetitive DNA: a fluid component of the Drosophila genome. Proceedings of the National Academy of Sciences of the USA 76, 62746279.Google Scholar