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Structure, molecular evolution and maintenance of copy number of extended repeated structures in the X-heterochromatin of Drosophila melanogaster

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Abstract

The 60 kb repeats located in the distal heterochromatin of the X chromosome of Drosophila melanogaster were cloned in overlapping cosmids. These regions, designated as SCLRs, comprised the following types of repeated elements Stellate genes, which are known to be involved in spermatogenesis; copia-like retrotransposons; LINE elements, including amplified Type rDNA insertions; and rDNA fragments. The following steps in SCLR formation were hypothesized: insertion of mobile elements into the rDNA and Stellate gene clusters: internal tandem duplication events; recombination between the rDNA cluster and Stellate tandem repeat; and amplification of the whole SCLR structure. There are about nine SCLR copies per haploid genome, but there is approximately a twofold variation in copy number between fly stocks. The SCLR copy number differences between closely related stocks are suggested to be the result of unequal sister chromatid exchange (USCE). The restricted variation in SCLR copy number between unrelated stocks and the absence of chromosomes free of SCLRs suggests that natural selection is active in copy number maintenance.

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References

  • Balakireva MD, Shevelyov YY, Nurminsky DI, Livak KJ, Gvozdev VA (1992) Structural organization and diversification of Y-linked sequences comprising Su(Ste) genes in Drosophila melanogaster. Nucleic Acids Res 20: 3731–3736

    Google Scholar 

  • Belyaeva ESp, Pasyukova EG, Glushkova IV, Iovleva OV, Kaidanov LZ, Gvozdev VA (1989) Hot spots of mdgl locations in chromosome 2 and fitness level in D. melanogaster stocks of common origin. Genetika (Russian) 25: 1047–1058

    Google Scholar 

  • Biessman H, Champion LE, O'Hair M, Ikenaga K, Kasravi B, Mason JM (1992) Frequent transpositions of Drosophila melanogaster HeT-A retrotransposons to receding chromosome ends. EMBO J 11: 4459–4469

    Google Scholar 

  • Caizzi R, Caggese C, Pimpinelli S (1993) Bari-1, a new transposon-like family in Drosophila melanogaster with a unique heterochromatic organization. Genetics 133: 335–345

    Google Scholar 

  • Danilevskaya ON, Kurenova EV, Pavlova MN, Bebehov DV, Link AJ, Koga A, Vellek A, Hartl DL (1991) He-T family DNA sequences in the Y chromosome of Drosophila melanogaster share homology with the X-linked Stellate genes. Chromosoma 100: 118–124

    Google Scholar 

  • Danilevskaya ON, Petrov DA, Pavlova MN, Koga A, Kurenova EV, Hartl DL (1992) Kepetitive DNA element, associated with telomeric sequences in D. melanogaster, contains open reading frames. Chromosoma 102: 32–40

    Google Scholar 

  • DiNocera PP (1988) Close relationship between non-viral retroposons in Drosophila melanogaster. Nucleic Acids Res 16: 4042–4052

    Google Scholar 

  • DiNocera PP, Dawid IB (1983) Interdigitated arrangement of two oligo(A)-terminated DNA sequences in Drosophila. Nucleic Acids Res 11: 5475–5483

    Google Scholar 

  • DiNocera PP, Graziani F, Lavorgna G (1986) Genomic and structural organization of Drosophila melanogaster G elements. Nucleic Acids Res 14: 675–691

    Google Scholar 

  • Hardy RW, Lindsley DL, Livak KJ, Lewis B, Siverstein L, Joslyn GL, Edvards J, Bonaccorsi S (1984) Cytogenetic analysis of segment of the Y chromosome of Drosophila melanogaster. Genetics 107: 591–610

    Google Scholar 

  • Hawley RS, Marcus CH (1989) Recombination controls of rDNA redundancy in Drosophila. Annu Rev, Genet 23: 87–120

    Google Scholar 

  • Heitz E (1933) Cytologisch Untersuchungen an Dipteren. III. Die somatische Heteropyknose bei Drosophila melanogaster und ihre genetische Bedeutung. Z Zellforsch 20: 237–287

    Google Scholar 

  • Jakubczak JL, Xiong Y, Eickbush TH (1990) Type I (RI) and Type II (R2) ribosomal DNA insertions of Drosophila melanogaster are retrotransposable elements closely related to those of Bombyx mori. J Mol Biol 212: 37–52

    Google Scholar 

  • Kaufmann BP (1934) Somatic mitoses of Drosophila melanogaster. J Morphol 56: 125–155

    Google Scholar 

  • Kidd SJ, Glover DM (1980) A DNA segment from D. melanogaster which contains five tandemly repeating units homologous to the major rDNA insertions. Cell 19: 103–119

    Google Scholar 

  • Lankenau DH, Huijser P, Jansen E, Miedema K, Hennig W (1989) DNA sequence comparison of micropia transposable elements from Drosophila hydei and Drosophila melanogaster. Chromosoma. 99: 111–117

    Google Scholar 

  • Lifshytz E, Hareven D (1982) Heterochromatin marks: a search for heterochromatin specific middle repetitive sequences in Drosophila. Chromosoma 86: 429–442

    Google Scholar 

  • Lindsley DL, Grell EH (1968) Genetic variations of Drosophila melanogaster. Carnegie Institution of Washington Publication no. 627

  • Livak KJ (1984) Organization and mapping of a sequence on the D. melanogaster X and Y chromosomes that is transcribed during spermatogenesis. Genetics 107: 611–634

    Google Scholar 

  • Livak KJ (1990) Detailed structure of the Drosophila melanogaster Stellate genes and their transcripts. Genetics 124: 303–316

    Google Scholar 

  • Lovett LA, Kaufmann TC, Mahowald AP (1980) A locus on the X chromosome apparently controlled by the Y chromosome during spermatogenesis in Drosophila melanogaster. Eur J Cell Biol 22: 49

    Google Scholar 

  • Lyckegaard EMS, Clark AG (1991) Evolution of ribosomal RNA gene copy number on the sex chromosomes of Drosophila melanogaster. Mol Biol Evol 8: 458–474

    Google Scholar 

  • Miklos GLG, Healy MJ, Pain P, Howeless AJ, Russel RJ (1984) Molecular and genetic studies on the euchromatin-heterochromatin transition near the uncoordinated (unc) locus. Chromosoma 89: 218–227

    Google Scholar 

  • Muller HJ, Painter TS (1932) The differentiation of the sex chromosomes of Drosophila into genetically active and inert regions. Z Induct Abstamm Vererbungslehre 62: 316–365

    Google Scholar 

  • Nurminsky DI (1993) Two subfamilies of mdgl retrotransposon with different evolutionary fates in Drosophila melanogaster. J Mol Evol 37: 496–503

    Google Scholar 

  • Pasuykova EC, Belyaeva ESp, Kogan GL, Kaidanov LZ, Gvozdev VA (1986) Concerted transpositions of mobile genetic elements coupled with fitness changes in Drosophila melanogaster. Mol Biol Evol 13: 299–312

    Google Scholar 

  • Pimpinelli S, Sullivan W, Prout M, Sandler L (1985) On biological functions mapping to the heterochromatin of Drosophila melanogaster. Genetics 109: 701–724

    Google Scholar 

  • Pimpinelli S, Bonaccorsi S, Gatti M, Sandler L (1986) The peculiar genetic organization of Drosophila heterochromatin. Trends Genet 2: 17–20

    Google Scholar 

  • Procunier JD, Tartof KD (1978) A genetic locus having trans and contiguous cis functions that control the disproportionate replication of ribosomal genes in Drosophila melanogaster Genetics 88: 67–79

    Google Scholar 

  • Rahman R, Lindsley DL (1981) Male-sterilising interactions between duplications and deficiences for proximal X-chromosome material in Drosophila melanogaster. Genetics 99: 49–64

    Google Scholar 

  • Ritossa FM, Atwood KC, Spiegelman SA (1966) Molecular explanation of the bobbed mutants of Drosophila as partial deficiences of “ribosomal” DNA. Genetics 54: 819–834

    Google Scholar 

  • Roiha H, Miller JR, Woods LC, Glover DM (1981) Arrangements and rearrangements of sequences flanking the two types of rRNA insertions in D. melanogaster. Nature 290: 749–753

    Google Scholar 

  • Sambrook J, Fritsch EF Maniatis T (1989) Molecular cloning, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Schneider I, Blumenthal AB (1978) Drosophila cell and tissue culture. In: Ashburner M, Wright TRF (eds) The genetics and biology of Drosophila, vol 2a. Academic Press, London, pp 366–316

    Google Scholar 

  • Shevelyov YY (1992) Copies of definite Stellate gene variant are located in the X-heterochromatin of Drosophila melanogaster and are probably expressed. Genetics 132: 1033–1037

    Google Scholar 

  • Shevelyov YY (1993) Non-mobile retrotransposon aurora in D. melanogaster heterochromatin. Mol Gen Genet 239: 205–208

    Google Scholar 

  • Shevelyov YY, Balakireva MD, Gvozdev VA (1989) Heterochromatic regions in different Drosophila melanogaster stocks contain similar arrangements of moderate repeats with inserted copia-like elements (MDG1). Chromosoma 98: 117–122

    Google Scholar 

  • Simeone A, La Volpe A, Boncinelli E (1985) Nucleotide sequence of a complete ribosomal spacer of Drosophila melanogaster. Nucleic Acids Res 13: 1089–1101

    Google Scholar 

  • Tolchkov EV, Balakireva MD, Alatortsev VE (1984) Inactivation of the X chromosome region with known fine genetic structure as a result of the variegated position effect in D. melanogaster. Genetika (Russian) 20: 1846–1856

    Google Scholar 

  • Tomkiel J Pimpinelli S, Sandler L (1991) Rescue from the abnormal oocyte maternal-effect lethality by ABO heterochromatin in Drosophila melanogaster. Genetics 128: 583–594

    Google Scholar 

  • Vaury C, Bucheton A, Pelisson A (1989) The beta-heterochromatin sequences flanking the I elements are themselves defective transposable elements. Chromosoma 98: 215–224

    Google Scholar 

  • Wu C-I, Lyttle TW, Wu M-L, Lin G-F (1988) Association between a satellite DNA sequence and the Responder of Segregation Distorter in D. melanogaster. Cell 54: 179–189

    Google Scholar 

  • Zabarovsky ER, Allikmets RL (1986) An improved technique for the efficient construction of gene libraries by partial filling-in of cohesive ends. Gene 42: 119–123

    Google Scholar 

Download references

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Nurminsky, D.I., Shevelyov, Y.Y., Nuzhdin, S.V. et al. Structure, molecular evolution and maintenance of copy number of extended repeated structures in the X-heterochromatin of Drosophila melanogaster . Chromosoma 103, 277–285 (1994). https://doi.org/10.1007/BF00352252

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  • DOI: https://doi.org/10.1007/BF00352252

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