Abstract
Telomeres at the ends of linear chromosomes of eukaryotes protect the chromosome termini from degradation and fusion. While telomeric replication/elongation mechanisms have been studied extensively, the functions of subterminal sequences are less well understood. In general, subterminal regions can be quite polymorphic, varying in size from organism to organism, and differing among chromosomes within an organism. The subterminal regions of Drosophila melanogaster are not well characterized today, and it is not known which and how many different components they contain. Here we present the molecular characterization of DNA components and their organization in the subterminal region of the left arm of chromosome 2 of the Oregon RC wildtype strain of D. melanogaster, including a minisatellite with a 457 bp repeat length. Two distinct polymorphic arrangements at 2L were found and analyzed, supporting the Drosophila telomere elongation model by retrotransposition. The high incidence of terminal chromosome deficiencies occurring in natural Drosophila populations is discussed in view of the telomere structure at 2L.
Similar content being viewed by others
References
Altschul SF, Gisg W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410
Ashburner M (1989) Drosophila, a laboratory manual. Cold Spring Harbor Press, Cold Spring Harbor, NY
Åslund L, Franzen L, Westin G, Persson T, Wigzell H, Petterson U (1985) Highly reiterated non-coding sequence in the genome of P. falciparum is composed of 21 base-pair tandem repeats. J Mol Biol 185: 509–516
Bachmann L, Raab M, Sperlich D (1990) Evolution of a telomere associated satellite DNA sequence in the genome of Drosophila tristis and related species. Genetica 83: 9–16
Bedbrook JR, Jones J, O'Dell M, Thompson RD, Flavell RB (1980a) A molecular description of telomeric heterochromatin in Secale species. Cell 19: 545–560
Bedbrook JR, O'Dell M, Flavell RB (1980b) Amplification of rearranged repeated DNA sequences in cereal plants. Nature 288: 133–137
Biessmann H, Mason JM (1988) Progressive loss of DNA sequences from terminal chromosome deficiencies in Drosophila melanogaster. EMBO J 7: 1081–1086
Biessmann H, Mason JM (1992) Genetics and molecular biology of telomeres. Adv Genet 30: 185–249
Biessmann H, Carter SB, Mason JM (1990a) Chromosome ends in Drosophila without telomeric DNA sequences. Proc Natl Acad Sci USA 87: 1758–1761
Biessmann H, Mason JM, Ferry K, d'Hulst M, Valgeirsdottir K, Traverse KL, Pardue ML (1990b) Addition of telomere-associated HeT DNA sequences “heals” broken chromosome ends in Drosophila. Cell 61: 663–673
Biessmann H, Champion LE, O'Hair M, Ikenaga K, Kasravi B, Mason JM (1992a) Frequent transpositions of Drosophila melanogaster HeT-A transposable elements to receding chromosome ends. EMBO J 11: 4459–4469
Biessmann H, Valgeirsdottir K, Lofsky A, Chin C, Ginther B, Levis RW, Pardue ML (1992b) HeT-A, a transposable element specifically involved in healing broken chromosome ends in Drosophila melanogaster. Mol Cell Biol 12: 3910–3918
Biessmann H, Kasravi B, Jakes K, Bui T, Ikenaga K, Mason JM (1993) The genomic organization of HeT-A retroposons in Drosophila melanogaster. Chromosoma 102: 297–305
Biessmann H, Kasravi B, Bui T, Fujiwara G, Champion LE, Mason JM (1994) Comparison of two active HeT-A retroposons of Drosophila melanogaster. Chromosoma 103: 90–98
Brown WR, MacKinnon PJ, Villasante A, Spurr N, Buckle VJ, Dobson MJ (1990) Structure and polymorphism of human telomere-associated DNA. Cell 63: 119–132
Burmeister M, Kim S, Price ER, Lange Tde, Tantravahi U, Myers RM, Cox DR (1991) A map of the distal region of the long arm of human chromosome 21 constructed by radiation hybrid mapping and pulsed-field gel electrophoresis. Genomics 9: 19–30
Carmona MJ, Morcillio G, Galler R, Martinez-Salas E, Campa AGde la, Edström JE (1985) Cloning and molecular characterization of a telomeric sequence from a temperature-induced Baliani ring. Chromosoma 92: 108–115
Cheng JF, Smith CL, Cantor CR (1989) Isolation and characterization of a human telomere. Nucleic Acids Res 17: 6109–6127
Cohn M, Edström JE (1991) Evolutionary relations between subtypes of telomere-associated repeats in Chironomus. J Mol Evol 32: 463–468
Cohn M, Edström JE (1992a) Chromosome ends in Chironomus pallidivittatus contain different subfamilies of telomere-associated repeats. Chromosoma 101: 634–640
Cohn M, Edström JE (1992b) Telomere-associated repeats in Chironomus form discrete subfamilies generated by gene conversion. J Mol Evol 35: 114–122
Cooke HJ, Brown WR, Rappold GA (1985) Hypervariable telomeric sequences from the human sex chromosomes are pseudoautosomal. Nature 317: 687–692
Corcoran LM, Thompson JK, Walliker D, Kemp DJ (1988) Homologous recombination within subtelomeric repeat sequences generates chromosome size polymorphisms in P. falciparum. Cell 53: 807–813
Danilevskaya ON, Petrov DA, Pavlova MN, Koga A, Kurenova EV, Hartl DL (1992) A repetitive DNA element, associated with telomeric sequences in Drosophila melanogaster, contains open reading frames. Chromosoma 102: 32–40
Danilevskaya O, Slot F, Pavlova M, Pardue ML (1994) Structure of the Drosophila HeT-A transposon: a retrotransposon-like element forming telomeres. Chromosoma 103: 215–224
Dorer DR, Henikoff S (1994) Expansions of transgene repeats cause heterochromatin formation and gene silencing in Drosophila. Cell 77: 993–1002
Ellis N, Goodfellow PN (1989) The mammalian pseudoautosomal region. Trends Genet 5: 406–410
Emery HS, Weiner AM (1981) An irregular satellite sequence is found at the termini of the linear extrachromosomal rDNA in Dictyostelium discoideum. Cell 26: 411–419
Foote SJ, Kemp DJ (1989) Chromosomes of malaria parasites. Trends Genet 5: 337–342
Gasser SM, Laemmli UK (1986) Cohabitation of scaffold binding regions with upstream/enhancer elements of three developmentally regulating genes of D. melanogaster. Cell 46: 521–530
Gehring WJ, Klemenz R, Weber U, Kloter U (1984) Functional analysis of the white +gene of Drosophila by P-factor-mediated transformation. EMBO J 3: 2077–2085
Gilson E, Laroche T, Gasser SM (1993) Telomeres and the functional architecture of the nucleus. Trends Cell Biol 3: 128–134
Golubovsky MD (1978) The “lethal giant larvae”-the most frequent second chromosome lethal in natural populations of D. melanogaster. Dros Inform Serv 53: 179
Golubovsky MD, Sokolova KB (1973) The expression and interaction of different alleles at the l(2)gl locus. Dros Inform Serv 50: 124
Green MM, Shepherd SH (1979) Genetic instability in Drosophila melanogaster: the induction of specific chromosome 2 deletions by MR elements. Genetics 92: 823–832
Guntaka RV, Gowda S, Rao AS, Green TJ (1985) Organization of Plasmodium falciparum genome. I. Evidence for a highly repeated DNA sequence. Nucleic Acids Res 13: 1965–1975
Hawley RS (1980) Chromosomal sites necessary for normal levels of meiotic recombination in Drosophila melanogaster. I. Evidence for and mapping of the sites. Genetics 94: 625–646
Hazelrigg T, Levis RW, Rubin GM (1984) Transformation of white locus DNA in Drosophila: dosage compensation, zeste interaction, and position effects. Cell 36: 469–481
Hinton T (1945) A study of chromosome ends in salivary gland nuclei of Drosophila. Biol Bull Woods Hole 88: 144–165
Hinton T, Atwood KC (1941) Terminal adhesions of salivary gland chromosomes in Drosophila. Proc Natl Acad Sci USA 27: 491–496
Horowitz H, Haber JE (1984) Subtelomeric regions of yeast chromosomes contain a 36 base-pair tandemly repeated sequence. Nucleic Acids Res 12: 7105–7121
Horowitz H, Thorburn P, Haber JE (1984) Rearrangements of highly polymorphic regions near telomeres of Saccharomyces cerevisiae. Mol Cell Biol 4: 2509–2517
Jacob L, Opper M, Metzroth B, Phannavong B, Mechler BM (1987) Structure of the l(2)gl gene of Drosophila and delimitation of its tumor suppressor domain. Cell 50: 215–225
Jeffreys AJ, Tamaki K, MacLeod A, Monckton DG, Neil DL, Armour JAL (1994) Complex gene conversion events in germline mutation at human minisatellites. Nature Genet 6: 136–145
Karpen GH, Spradling AC (1992) Analysis of subtelomeric heterochromatin in the Drosophila minichromosome Dp 1187 by single-P element insertional mutagenesis. Genetics 132: 737–753
Kaufmann BP, Gay H (1969) The capacity of the fourth chromosome of Drosophila melanogaster to establish end-to-end contacts with the other chromosomes in salivary gland cells. Chromosoma 26: 395–409
Lange Tde, Shine L, Myers RM, Cox DR, Naylor SL, Killery AM, Varmus HE (1990) Structure and variability of human chromosome ends. Mol Cell Biol 10: 518–527
Levis R, Hazelrigg T, Rubin GM (1985) Effects of genome position on the expression of transduced copies of the white gene of Drosophila. Science 229: 558–561
Levis RW (1989) Viable deletions of a telomere from a Drosophila chromosome. Cell 58: 791–801
Levis RW, Ganesan R, Houtchens K, Tolar LA, Sheen FM (1993) Transposons in place of telomeric repeats at a Drosophila telomere. Cell 75: 1083–1093
Lundblad V, Blackburn EH (1993) An alternative pathway for yeast telomere maintenance rescues est 1-senescence. Cell 73: 347–360
Maguire M (1984) The mechanism of meiotic homologue pairing. J Theor Biol 106: 605–615
Mason JM, Biessmann H (1995) The unusual telomeres of Drosophila. Trends Genet 11: 58–62
Mason JM, Strobel E, Green MM (1984) mu-2: Mutator gene in Drosophila that potentiates the induction of terminal deficiencies. Proc Natl Acad Sci USA 81: 6090–6094
Mechler BM, McGinnis W, Gehring WJ (1985) Molecular cloning of lethal(2) giant larvae, a recessive oncogene of Drosophila melanogaster. EMBO J 4: 1551–1557
Myerowitz EM, Hogness DS (1982) Molecular organization of a Drosophila puff site that responds to ecdysone. Cell 28: 165–178
Nielsen L, Edström JE (1993) Complex telomere-associated repeat units in members of the genus Chironomus evolve from sequences similar to simple telomeric repeats. Mol Cell Biol 13: 1583–1589
Nielsen L, Schmidt ER, Edström JE (1990) Subrepeats result from regional DNA sequence conservation in tandem repeats in Chironomus telomeres. J Mol Biol 216: 577–584
Oquendo P, Goman M, Mackay M, Langsley G, Walliker D, Scaife J (1986) Characterisation of a repetitive DNA sequence from the malaria parasite, Plasmodium falciparum. Mol Biochem Parasitol 18: 89–101
Pace T, Ponzi M, Dore E, Frontali C (1987) Telomeric motifs are present in a highly repetitive element in the Plasmodium berghei genome. Mol Biochem Parasitol 24: 193–202
Pace T, Ponzi M, Dore E, Janse C, Mons B, Frontali C (1990) Long insertions within telomeres contribute to chromosome size polymorphism in Plasmodium berghei. Mol Cell Biol 10: 6759–6764
Pereira A, Doshen J, Tanaka E, Goldstein LSB (1992) Genetic analysis of a Drosophila microtubule-associated protein. J Cell Biol 116: 377–383
Rappold G, Willson TA, Henke A, Gough NM (1992) Arrangement and localization of the human GM-CSF receptor α chain gene CSF2RA within the X-Y pseudoautosomal region. Genomics 14: 455–461
Rouyer F, Chapelle Ade la, Andersson M, Weissenbach J (1990) An interspersed repeated sequence specific for human subtelomeric regions. EMBO J 9: 505–514
Saiga H, Edström JE (1985) Long tandem arrays of complex repeat units in Chironomus telomeres. EMBO J 4: 799–804
Scherer G, Tschudi C, Perera J, Delius H, Pirrotta V (1983) B104, a new dispersed repeated gene family in Drosophila melanogaster and its analogies with retroviruses. J Mol Biol 157: 435–451
Sheen FM, Levis RW (1994) Transposition of the LINE-like retrotransposon TART to Drosophila chromosome termini. Proc Natl Acad Sci USA 91: 12510–12514
Simmler M-C, Rouyer F, Vergnaud G, Nyström-Lahti M, Ngo KY, Chapelle Ade la, Weissenbach J (1985) Pseudoautosomal DNA sequences in the pairing region of the human sex chromosomes. Nature 317: 692–697
Simmler MC, Johnsson C, Petit C, Rouyer F, Vergnaud G, Weissenbach J (1987) Two highly polymorphic minisatellites from the pseudoautosomal region of the human sex chromosomes. EMBO J 6: 963–969
Tower J, Karpen GH, Craig N, Spradling AC (1993) Preferential transposition of Drosophila P elements to nearby chromosomal sites. Genetics 133: 347–359
Wallrath LL, Elgin SCR (1995) Position effect variegation in Drosophila is associated with an altered chromatin structure. Genes Dev 9: 1263–1277
Wertman KF, Wyman AR, Botstein D (1986) Host/vector interactions which affect the viability of recombinant phage lambda clones. Gene 49: 253–262
Wilkie AO, Higgs DR, Rach KA, Buckle VJ, Spurr NK, Fischel-Ghodsian N, Ceccherini I, Brown WR, Harris PC (1991) Stable length polymorphism of up to 260 kb at the tip of the short arm of human chromosome 16. Cell 64: 595–606
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Walter, M.F., Jang, C., Kasravi, B. et al. DNA organization and polymorphism of a wild-type Drosophila telomere region. Chromosoma 104, 229–241 (1995). https://doi.org/10.1007/BF00352254
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00352254