Abstract
A homogeneous array of 80 tandem repeats of the Bari1 transposon is located in the pericentromeric h39 region of chromosome 2 of Drosophila melanogaster. Here, we report that the Bari1 cluster is interrupted by an 8556-bp insertion. DNA sequencing and database searches identified this insertion as a previously unannotated retrotransposon that we have named MAX. MAX possesses two ORFs; ORF1 putatively encodes a polyprotein comprising GAG and RT domains, while ORF2 could encode a 288-amino acid protein of unknown function. Alignment with the RT domains of known LTR retrotransposons shows that MAX belongs to the BEL-Pao family, which remarkable for its widespread presence in different taxa, including lower chordates. We have analyzed the distribution of MAX elements within representative species of the Sophophora subgroup and found that they are restricted to the species of the melanogaster complex, where they are heavily represented in the heterochromatin of all autosomes and on the Y chromosome.
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References
Arkhipova IR, Lyubomirskaya NV, Ilyin Yu (1995) Drosophila retrotransposons. Springer-Verlag, Heidelberg, Germany
Bao Z, Eddy SR (2002) Automated de novo identification of repeat sequence families in sequenced genomes. Genome Res 12:1269–1276
Bartolomé C, Maside X, Charlesworth B (2002) On the abundance and distribution of transposable elements in the genome of Drosophila melanogaster. Mol Biol Evol 19:926–937
Berezikov E, Bucheton A, Busseau I (2000) Non-LTR retrotransposons in the genome of Drosophila melanogaster. Genome Biol 1:research0011.1–0011.15
Bowen NJ, McDonald JF (1999) Genomic analysis of Caenorhabditis elegans reveals ancient families of retroviral-like elements. Genome Res 9:924–935
Bowen NJ, McDonald JF (2001) Drosophila euchromatic LTR retrotransposons are much younger than the host species in which they reside. Genome Res 11:1527–1540
Britten RJ (1996) DNA sequence insertion and evolutionary variation in gene regulation. Proc Natl Acad Sci USA 93:9374–9377
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
Capy P (1998) A plastic genome. Nature 396:522–523
Covey SN (1986) Amino acid homology in gag region of reverse transcribing elements and the coat protein of cauliflower mosaic virus. Nucleic Acids Res 14:623–635
Craig NL, Craigie R, Gellert M, Lambowitz AM (eds) (2002) Mobile DNA II. ASM Press, Washington, D.C.
Felder H, Herzceg A, de Chastonay Y, Aeby P, Tobler H, Muller F (1994) Tas, a retrotransposon from the parasitic nematode Ascaris lumbricoides. Gene 149:219–225
Flavell A (1986) Transposon tricks revealed. Nature 320:397
Gatti M, Bonaccorsi S, Pimpinelli S (1994) Looking at Drosophila mitotic chromosomes. Methods Cell Biol 44:371–391
Hochstenbach R, Harhangi H, Schouren K, Hennig W (1994) Degenerating gypsy retrotransposons in male fertility gene on the Y chromosome of Drosophila hydei. J Mol Evol 39:452–465
Hoskins RA, et al (2002) Heterochromatic sequences in a Drosophila whole-genome shotgun assembly. Genome Biol 3:research0085.1–0085.16
Kaminker JS, Bergman CM, Kronmiller B, Carlson J, Svirskas R, Patel S, Frise E, Wheeler DA, Lewis SE, Rubin GM, Ashburner M, Celniker SE (2002) The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective. Genome Biol 3:research0084.1–0084.20
Kidwell MG, Lisch D (2001) Perspective: Transposable elements, parasitic DNA, and genome evolution. Evolution 55:1–24
Kim JM, Vanguri S, Boeke JD, Gabriel A, Voytas DF (1998) Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res 8:464–478
Kogan GL, Tulin AV, Aravin AA, Abramov YA, Kalmykova AI, Maisonhaute C, Gvozdev VA (2003) The GATE retrotransposon in Drosophila melanogaster: mobility in heterochromatin and aspects of its expression in germline tissues. Mol Genet Genomics 269:234–242
Malik HS, Henikoff S, Eickbush TH (2000) Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses. Genome Res 10:1307–1318
Marsano RM, Moschetti R, Barsanti P, Caggese C, Caizzi R (2003) A survey of DNA sequences surrounding the Bari 1 repeats in the pericentromeric h39 region of Drosophila melanogaster. Gene 307:167–174
McDonald JF (1993) Evolution and consequences of transposable elements. Curr Opin Genet Dev 3:855–864
McDonald JF (1998) Transposable elements, gene silencing and macroevolution. Trends Ecol Evol 13:94–95
McDonald JF, Matyunina LV, Wilson S, Jordan IK, Bowen NG, Miller WJ (1997) LTR retrotransposons and the evolution of eukaryotic enhancers. Genetica 100:3–13
Nagaki K, Song J, Stupar RM, Parokonny AS, Yuan Q, Ouyang S, Liu J, Hsiao J, Jones KM, Dawe RK, Buell CR, Jiang J (2003) Molecular and cytological analyses of a large tracks of centromeric DNA reveal the structure and evolutionary dynamics of maize centromeres. Genetics 163:759–770
Pardue ML (1986) In-situ hybridization to DNA of chromosomes and nuclei. In: Roberts B (ed) Drosophila: a practical approach. IRL Press, Oxford, pp 111–137
Peifer M, Bender M (1988) Sequences of the gypsy transposon of Drosophila necessary for its effects on adjacent genes. Proc Natl Acad Sci USA 85:9650–9654
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. Proc Natl Acad Sci USA 92:3804–3808
SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768
SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45
Song SU, Gerasimova T, Kurkulos M, Boeke JD, Corces VG (1994) An env -like protein encoded by a Drosophila retroelement: evidence that gypsy is an infectious retrovirus. Genes Dev 8:2046–2057
Sun X, Le HD, Wahlstrom JM, Karpen GH (2003) Sequence analysis of a functional Drosophila centromere. Genome Res 13:182–194
Szak ST, Pickeral OK, Makalowski W, Boguski MS, Landsman D, Boeke JD (2002) Molecular archeology of L1 insertions in the human genome. Genome Biol 3:research0052.1–0052.18
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 15:4876–4882
Tulin AV, Kogan GL, Filipp D, Balakireva MD, Gvozdev VA (1997) Heterochromatic Stellate gene cluster in Drosophila melanogaster: structure and molecular evolution. Genetics 146:253–262
Vaury C, Bucheton A, Pelisson A (1989) The β-heterochromatin sequences flanking the I elements are themselves defective transposable elements. Chromosoma 98:215–224
Xiong Y, Eickbush TH (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 10:3353–3362
Yoder JA, Walsh CP, Bestor TH (1997) Cytosine methylation and the ecology of intragenomic parasites. Trends Genet 13:335–340
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This work was supported by a grant from the Ministero dell’Istruzione e della Ricerca Scientifica (PRIN2002) to R.C.
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Communicated by G. P. Georgiev
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Marsano, R.M., Marconi, S., Moschetti, R. et al. MAX, a novel retrotransposon of the BEL-Pao family, is nested within the Bari 1 cluster at the heterochromatic h39 region of chromosome 2 in Drosophila melanogaster . Mol Genet Genomics 270, 477–484 (2004). https://doi.org/10.1007/s00438-003-0947-7
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DOI: https://doi.org/10.1007/s00438-003-0947-7