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Subtelomeres pp 211–225Cite as

Subtelomeres in Drosophila and Other Diptera

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Abstract

While Drosophila telomeres are considered unusual, because they lack short, telomerase-generated telomeric repeat, in other ways they are similar to telomeres found in most eukaryotes. Subtelomeric repeated DNA sequences, for example, exist between the terminal DNA array and the unique sequences found in the euchromatic chromosome arms. Subtelomeric sequences in Drosophila consist of complex repeat motifs that are shared among chromosome ends, although the arrangement of the motifs varies considerably. While these motifs diverge rapidly, similarities can still be found in sibling species. Surprisingly, the subtelomeres seem to be able to communicate with the rest of the genome; deletions of the 2L subtelomere suppress telomere position effect at other chromosome ends, and insertions of transposable elements into the XL subtelomere can silence homologous sequences in an RNAi-dependent manner. While Drosophila telomeres are maintained by targeted transposition of a small group of retrotransposons, telomeres in nematoceran flies seem to be maintained by gene conversion among telomeric sequences that in many ways resemble complex subtelomeric repeats.

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References

  • Abad, J. P., de Pablos, B., Osoegawa, K., de Jong, P. J., Martin-Gallardo, A., et al. (2004). Genomic analysis of Drosophila melanogaster telomeres: Full-length copies of HeT-A and TART elements at telomeres. Molecular Biology and Evolution, 21, 1613–1619.

    Article  CAS  PubMed  Google Scholar 

  • Anderson, J. A., Song, Y. S., & Langley, C. H. (2008). Molecular population genetics of Drosophila subtelomeric DNA. Genetics, 178, 477–487.

    Article  CAS  PubMed  Google Scholar 

  • Andreyeva, E. N., Belyaeva, E. S., Semeshin, V. F., Polkholkova, G. V., & Zhimulev, I. F. (2005). Three distinct chromatin domains in telomere ends of polytene chromosomes in Drosophila melanogaster Tel mutants. Journal of Cell Science, 118, 5465–5477.

    Article  CAS  PubMed  Google Scholar 

  • Biessmann, H., Zurovcova, M., Yao, J. G., Lozovskaya, E., & Walter, M. F. (2000). A telomeric satellite in Drosophila virilis and its sibling species. Chromosoma, 109, 372–380.

    Article  CAS  PubMed  Google Scholar 

  • Biessmann, H., Prasad, S., Walter, M. F., & Mason, J. M. (2005). Euchromatic and heterochromatic domains at Drosophila telomeres. Biochemistry and Cell Biology, 83, 477–485.

    Article  CAS  PubMed  Google Scholar 

  • Boivin, A., Gally, C., Netter, S., Anxolabehere, D., & Ronsseray, S. (2003). Telomere associated sequences of Drosophila recruit Polycomb-group proteins in vivo and can induce pairing-sensitive repression. Genetics, 164, 195–208.

    CAS  PubMed  Google Scholar 

  • Broun, P., Ganal, M. W., & Tanksley, S. D. (1992). Telomeric arrays display high levels of heritable polymorphism among closely related plant varieties. Proceedings of the National Academy of Sciences of the United States of America, 89, 1354–1357.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brown, W. R., MacKinnon, P. J., Villasante, A., Spurr, N., Buckle, V. J., et al. (1990). Structure and polymorphism of human telomere-associated DNA. Cell, 63, 119–132.

    Article  CAS  PubMed  Google Scholar 

  • Capkova Frydrychova, R., Biessmann, H., Konev, A. Y., Golubovsky, M. D., Johnson, J., et al. (2007). Transcriptional activity of the telomeric retrotransposon HeT-A in Drosophila melanogaster is stimulated as a consequence of subterminal deficiencies at homologous and nonhomologous telomeres. Molecular and Cellular Biology, 27, 4991–5001.

    Article  Google Scholar 

  • Capkova Frydrychova, R., Mason, J. M., & Archer, T. K. (2008). HP1 is distributed within distinct chromatin domains at telomeres. Genetics, 180, 121–131.

    Article  Google Scholar 

  • Clark, A. G., Eisen, M. B., Smith, D. R., Bergman, C. M., Oliver, B., et al. (2007). Evolution of genes and genomes on the Drosophila phylogeny. Nature, 450, 203–218.

    Article  PubMed  Google Scholar 

  • Cryderman, D. E., Morris, E. J., Biessmann, H., Elgin, S. C. R., & Wallrath, L. L. (1999). Silencing at Drosophila telomeres: Nuclear organization and chromatin structure play critical roles. EMBO Journal, 18, 3724–3735.

    Article  CAS  PubMed  Google Scholar 

  • Engels, W. R. (1979). Extrachromosomal control of mutability in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 76, 4011–4015.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Filion, G. J., van Bemmel, J. G., Braunschweig, U., Talhout, W., Kind, J., et al. (2010). Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell, 143, 212–224.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Frydrychova, R., Grossmann, P., Trubac, P., Vitkova, M., & Marec, F. E. (2004). Phylogenetic distribution of TTAGG telomeric repeats in insects. Genome, 47, 163–178.

    Article  CAS  PubMed  Google Scholar 

  • Gao, G. J., Walser, J. C., Beaucher, M. L., Morciano, P., Wesolowska, N., et al. (2010). HipHop interacts with HOAP and HP1 to protect Drosophila telomeres in a sequence-independent manner. EMBO Journal, 29, 819–829.

    Article  CAS  PubMed  Google Scholar 

  • Golubovsky, M. D., Konev, A. Y., Walter, M. F., Biessmann, H., & Mason, J. M. (2001). Terminal retrotransposons activate a subtelomeric white transgene at the 2L telomere in Drosophila. Genetics, 158, 1111–1123.

    CAS  PubMed  Google Scholar 

  • Grimaud, C., Bantignies, F., Pal-Bhadra, M., Ghana, P., Bhadra, U., et al. (2006). RNAi components are required for nuclear clustering of Polycomb group response elements. Cell, 124, 957–971.

    Article  CAS  PubMed  Google Scholar 

  • Haley, K. J., Stuart, J. R., Raymond, J. D., Niemi, J. B., & Simmons, M. J. (2005). Impairment of cytotype regulation of P-element activity in Drosophila melanogaster by mutations in the Su(var)205 gene. Genetics, 171, 583–595.

    Article  CAS  PubMed  Google Scholar 

  • Josse, T., Teysset, L., Todeschini, A. L., Sidor, C. M., Anxolabehere, D., et al. (2007). Telomeric trans-silencing: An epigenetic repression combining RNA silencing and heterochromatin formation. PLoS Genetics, 3, 1633–1643.

    Article  CAS  PubMed  Google Scholar 

  • Karpen, G. H., & Spradling, A. C. (1992). Analysis of subtelomeric heterochromatin in the Drosophila minichromosome Dp1187 by single P element insertional mutagenesis. Genetics, 132, 737–753.

    CAS  PubMed  Google Scholar 

  • Kass-Eisler, A., & Greider, C. W. (2000). Recombination in telomere-length maintenance. Trends in Biochemical Sciences, 25, 200–206.

    Article  CAS  PubMed  Google Scholar 

  • Kern, A. D., & Begun, D. J. (2008). Recurrent deletion and gene presence/absence polymorphism: Telomere dynamics dominate evolution at the tip of 3L in Drosophila melanogaster and D. simulans. Genetics, 179, 1021–1027.

    Article  CAS  PubMed  Google Scholar 

  • Kurenova, E., Champion, L., Biessmann, H., & Mason, J. M. (1998). Directional gene silencing induced by a complex subtelomeric satellite from Drosophila. Chromosoma, 107, 311–320.

    Article  CAS  PubMed  Google Scholar 

  • Louis, E. J., & Haber, J. E. (1992). The structure and evolution of subtelomeric-Y′ repeats in Saccharomyces cerevisiae. Genetics, 131, 559–574.

    CAS  PubMed  Google Scholar 

  • Madalena, C. R. G., & Gorab, E. (2005). A chromosome end satellite of Rhynchosciara americana (Diptera: Sciaridae) resembling nematoceran telomeric repeats. Insect Molecular Biology, 14, 255–262.

    Article  CAS  PubMed  Google Scholar 

  • Madalena, C. R. G., Amabis, J. M., & Gorab, E. (2010). Unusually short tandem repeats appear to reach chromosome ends of Rhynchosciara americana (Diptera: Sciaridae). Chromosoma, 119, 613–623.

    Article  PubMed  Google Scholar 

  • Marin, L., Lehmann, M., Nouaud, D., Hassan, I., Anxolabéhère, D., et al. (2000). P-element repression in Drosophila melanogaster by a naturally occurring defective telomeric P copy. Genetics, 155, 1841–1854.

    CAS  PubMed  Google Scholar 

  • Mason, J. M., Konev, A. Y., & Biessmann, H. (2003). Telomeric position effect in Drosophila melanogaster reflects a telomere length control mechanism. Genetica, 117, 319–325.

    Article  CAS  PubMed  Google Scholar 

  • Mason, J. M., Ransom, J., & Konev, A. Y. (2004). A deficiency screen for dominant suppressors of telomeric silencing in Drosophila. Genetics, 168, 1353–1370.

    Article  CAS  PubMed  Google Scholar 

  • Mason, J. M., Frydrychova, R. C., & Biessmann, H. (2008). Drosophila telomeres: An exception providing new insights. BioEssays, 30, 25–37.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mason, J. M., Reddy, H. K., & Capkova Frydrychova, R. (2011). Telomere maintenance in organisms without telomerase. In H. Seligmann (Ed.), DNA replication: Current advances. Rijeka: InTech.

    Google Scholar 

  • Mechler, B. M., McGinnis, W., & Gehring, W. J. (1985). Molecular cloning of lethal(2)giant larvae, a recessive oncogene of Drosophila melanogaster. EMBO Journal, 4, 1551–1557.

    CAS  PubMed  Google Scholar 

  • Mefford, H. C., & Trask, B. J. (2002). The complex structure and dynamic evolution of human subtelomeres. Nature Reviews Genetics, 3, 91–102.

    Article  CAS  PubMed  Google Scholar 

  • Melnikova, L., & Georgiev, P. (2005). Drosophila telomeres: The non-telomerase alternative. Chromosome Research, 13, 431–441.

    Article  CAS  PubMed  Google Scholar 

  • Phalke, S., Nickel, O., Walluscheck, D., Hortig, F., Onorati, M. C., et al. (2009). Retrotransposon silencing and telomere integrity in somatic cells of Drosophila depends on the cytosine-5 methyltransferase DNMT2. Nature Genetics, 41, 696–702.

    Article  CAS  PubMed  Google Scholar 

  • Raffa, G. D., Siriaco, G., Cugusi, S., Ciapponi, L., Cenci, G., et al. (2009). The Drosophila modigliani (moi) gene encodes a HOAP-interacting protein required for telomere protection. Proceedings of the National Academy of Sciences of the United States of America, 106, 2271–2276.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Raffa, G. D., Raimondo, D., Sorino, C., Cugusi, S., Cenci, G., et al. (2010). Verrocchio, a Drosophila OB fold-containing protein, is a component of the terminin telomere-capping complex. Genes & Development, 24, 1596–1601.

    Article  CAS  Google Scholar 

  • Reiss, D., Josse, T., Anxolabehere, D., & Ronsseray, S. (2004). aubergine mutations in Drosophila melanogaster impair P cytotype determination by telomeric P elements inserted in heterochromatin. Molecular Genetics and Genomics, 272, 336–343.

    Article  CAS  PubMed  Google Scholar 

  • Riddle, N. C., Minoda, A., Kharchenko, P. V., Alekseyenko, A. A., Schwartz, Y. B., et al. (2011). Plasticity in patterns of histone modifications and chromosomal proteins in Drosophila heterochromatin. Genome Research, 21, 147–163.

    Article  CAS  PubMed  Google Scholar 

  • Roche, S. E., & Rio, D. C. (1998). Trans-silencing by P elements inserted in subtelomeric heterochromatin involves the Drosophila Polycomb group gene, Enhancer of zeste. Genetics, 149, 1839–1855.

    CAS  PubMed  Google Scholar 

  • Ronsseray, S., Lehmann, M., Nouaud, D., & Anxolabehere, D. (1997). P element regulation and X-chromosome subtelomeric heterochromatin in Drosophila melanogaster. Genetica, 100, 95–107.

    Article  CAS  PubMed  Google Scholar 

  • Ronsseray, S., Josse, T., Boivin, A., & Anxolabehere, D. (2003). Telomeric transgenes and trans-silencing in Drosophila. Genetica, 117, 327–335.

    Article  CAS  PubMed  Google Scholar 

  • Rossato, R. M., Madalena, C. R. G., & Gorab, E. (2007). Unusually short tandem repeats in the chromosome end structure of Rhynchosciara (Diptera: Sciaridae). Genetica, 131, 109–116.

    Article  CAS  PubMed  Google Scholar 

  • Savitsky, M., Kwon, D., Georgiev, P., Kalmykova, A., & Gvozdev, V. (2006). Telomere elongation is under the control of the RNAi-based mechanism in the Drosophila germline. Genes & Development, 20, 345–354.

    Article  CAS  Google Scholar 

  • Schmid, K. J., & Tautz, D. (1997). A screen for fast evolving genes from Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 94, 9746–9750.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shanower, G. A., Muller, M., Blanton, J. L., Honti, V., Gyurkovics, H., et al. (2005). Characterization of the grappa gene, the Drosophila histone H3 lysine 79 methyltransferase. Genetics, 169, 173–184.

    Article  CAS  PubMed  Google Scholar 

  • Siriaco, G. M., Cenci, G., Haoudi, A., Champion, L. E., Zhou, C., et al. (2002). Telomere elongation (Tel), a new mutation in Drosophila melanogaster that produces long telomeres. Genetics, 160, 235–245.

    CAS  PubMed  Google Scholar 

  • Stuart, J. R., Haley, K. J., Swedzinski, D., Lockner, S., Kocian, P. E., et al. (2002). Telomeric P elements associated with cytotype regulation of the P transposon family in Drosophila melanogaster. Genetics, 162, 1641–1654.

    CAS  PubMed  Google Scholar 

  • Villasante, A., Abad, J. P., Planello, R., Mendez-Lago, M., Celniker, S. E., et al. (2007). Drosophila telomeric retrotransposons derived from an ancestral element that was recruited to replace telomerase. Genome Research, 17, 1909–1918.

    Article  CAS  PubMed  Google Scholar 

  • Walter, M. F., Jang, C., Kasravi, B., Donath, J., Mechler, B. M., et al. (1995). DNA organization and polymorphism of a wild-type Drosophila telomere region. Chromosoma, 104, 229–241.

    Article  CAS  PubMed  Google Scholar 

  • Wiegmann, B. M., Trautwein, M. D., Kim, J. W., Cassel, B. K., Bertone, M. A., et al. (2009). Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. BMC Biology, 7, 34.

    Article  PubMed Central  PubMed  Google Scholar 

  • Wiegmann, B. M., Trautwein, M. D., Winkler, I. S., Barr, N. B., Kim, J. W., et al. (2011). Episodic radiations in the fly tree of life. Proceedings of the National Academy of Sciences of the United States of America, 108, 5690–5695.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

JMM was supported by the Intramural Research Program, US National Institutes of Health. AV was supported by the Ministerio de Economia y Competitividad (BFU2011-30295-C02-01) and an institutional grant from Fundación Ramón Areces to the CBMSO.

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Correspondence to James M. Mason .

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Mason, J.M., Villasante, A. (2014). Subtelomeres in Drosophila and Other Diptera. In: Louis, E., Becker, M. (eds) Subtelomeres. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-41566-1_12

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