Skip to main content
PMC home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1993 May 11;21(9):2117–2123. doi: 10.1093/nar/21.9.2117

Pao, a highly divergent retrotransposable element from Bombyx mori containing long terminal repeats with tandem copies of the putative R region.

Y Xiong 1, W D Burke 1, T H Eickbush 1
PMCID: PMC309473  PMID: 8389039

Abstract

Analysis of aberrant ribosomal DNA (rDNA) repeats of Bombyx mori resulted in the discovery of a 4.8 kilobase retrotransposable element, Pao. Approximately 40 copies of Pao are present in the genome with most located outside the rDNA units. The complete sequence of one Pao element and partial sequence of four other copies indicated that Pao encodes an 1158 amino acid open-reading frame (ORF). Located within this ORF are domains with sequence similarity to retroviral gag genes, aspartic protease and reverse transcriptase. RNase H and integrase domains were not identified suggesting that the cloned copies were not full-length elements. Pao elements contain long terminal repeats (LTRs) with a central region composed of variable numbers of 46 bp tandem repeats. The variable region appears to correspond to the R region of retroviral LTRs, the region responsible for strand transfer during reverse transcription. Based on a sequence analysis of its reverse transcriptase domain, Pao is most similar to TAS of Ascaris lumbricoides. Pao and TAS represent a subgroup of LTR retrotransposons distinct from the Copia-Ty1 and Gypsy-Ty3 subgroups.

Full text

PDF
2122

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aeby P., Spicher A., de Chastonay Y., Müller F., Tobler H. Structure and genomic organization of proretrovirus-like elements partially eliminated from the somatic genome of Ascaris lumbricoides. EMBO J. 1986 Dec 1;5(12):3353–3360. doi: 10.1002/j.1460-2075.1986.tb04650.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Boeke J. D., Corces V. G. Transcription and reverse transcription of retrotransposons. Annu Rev Microbiol. 1989;43:403–434. doi: 10.1146/annurev.mi.43.100189.002155. [DOI] [PubMed] [Google Scholar]
  3. Bucheton A. I transposable elements and I-R hybrid dysgenesis in Drosophila. Trends Genet. 1990 Jan;6(1):16–21. doi: 10.1016/0168-9525(90)90044-7. [DOI] [PubMed] [Google Scholar]
  4. Burke W. D., Calalang C. C., Eickbush T. H. The site-specific ribosomal insertion element type II of Bombyx mori (R2Bm) contains the coding sequence for a reverse transcriptase-like enzyme. Mol Cell Biol. 1987 Jun;7(6):2221–2230. doi: 10.1128/mcb.7.6.2221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Camirand A., Brisson N. The complete nucleotide sequence of the Tst1 retrotransposon of potato. Nucleic Acids Res. 1990 Aug 25;18(16):4929–4929. doi: 10.1093/nar/18.16.4929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cappello J., Handelsman K., Lodish H. F. Sequence of Dictyostelium DIRS-1: an apparent retrotransposon with inverted terminal repeats and an internal circle junction sequence. Cell. 1985 Nov;43(1):105–115. doi: 10.1016/0092-8674(85)90016-9. [DOI] [PubMed] [Google Scholar]
  7. Christy R. J., Brown A. R., Gourlie B. B., Huang R. C. Nucleotide sequences of murine intracisternal A-particle gene LTRs have extensive variability within the R region. Nucleic Acids Res. 1985 Jan 11;13(1):289–302. doi: 10.1093/nar/13.1.289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Clare J., Farabaugh P. Nucleotide sequence of a yeast Ty element: evidence for an unusual mechanism of gene expression. Proc Natl Acad Sci U S A. 1985 May;82(9):2829–2833. doi: 10.1073/pnas.82.9.2829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Coletta M., Amiconi G., Bellelli A., Bertollini A., Carsky J., Castagnola M., Condò S., Brunori M. Alteration of T-state binding properties of naturally glycated hemoglobin, HbA1c. J Mol Biol. 1988 Sep 5;203(1):233–239. doi: 10.1016/0022-2836(88)90104-0. [DOI] [PubMed] [Google Scholar]
  10. Covey S. N. Amino acid sequence homology in gag region of reverse transcribing elements and the coat protein gene of cauliflower mosaic virus. Nucleic Acids Res. 1986 Jan 24;14(2):623–633. doi: 10.1093/nar/14.2.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Doolittle R. F., Feng D. F., Johnson M. S., McClure M. A. Origins and evolutionary relationships of retroviruses. Q Rev Biol. 1989 Mar;64(1):1–30. doi: 10.1086/416128. [DOI] [PubMed] [Google Scholar]
  12. Eickbush T. H., Kafatos F. C. A walk in the chorion locus of Bombyx mori. Cell. 1982 Jun;29(2):633–643. doi: 10.1016/0092-8674(82)90179-9. [DOI] [PubMed] [Google Scholar]
  13. Eickbush T. H., Robins B. Bombyx mori 28S ribosomal genes contain insertion elements similar to the Type I and II elements of Drosophila melanogaster. EMBO J. 1985 Sep;4(9):2281–2285. doi: 10.1002/j.1460-2075.1985.tb03927.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Eickbush T. H. Transposing without ends: the non-LTR retrotransposable elements. New Biol. 1992 May;4(5):430–440. [PubMed] [Google Scholar]
  15. Evgen'ev M. B., Corces V. G., Lankenau D. H. Ulysses transposable element of Drosophila shows high structural similarities to functional domains of retroviruses. J Mol Biol. 1992 Jun 5;225(3):917–924. doi: 10.1016/0022-2836(92)90412-d. [DOI] [PubMed] [Google Scholar]
  16. Fourcade-Peronnet F., d'Auriol L., Becker J., Galibert F., Best-Belpomme M. Primary structure and functional organization of Drosophila 1731 retrotransposon. Nucleic Acids Res. 1988 Jul 11;16(13):6113–6125. doi: 10.1093/nar/16.13.6113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Friesen P. D., Nissen M. S. Gene organization and transcription of TED, a lepidopteran retrotransposon integrated within the baculovirus genome. Mol Cell Biol. 1990 Jun;10(6):3067–3077. doi: 10.1128/mcb.10.6.3067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Grandbastien M. A., Spielmann A., Caboche M. Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature. 1989 Jan 26;337(6205):376–380. doi: 10.1038/337376a0. [DOI] [PubMed] [Google Scholar]
  19. Hansen L. J., Chalker D. L., Sandmeyer S. B. Ty3, a yeast retrotransposon associated with tRNA genes, has homology to animal retroviruses. Mol Cell Biol. 1988 Dec;8(12):5245–5256. doi: 10.1128/mcb.8.12.5245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hibner B. L., Burke W. D., Eickbush T. H. Sequence identity in an early chorion multigene family is the result of localized gene conversion. Genetics. 1991 Jul;128(3):595–606. doi: 10.1093/genetics/128.3.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Holton T. A., Graham M. W. A simple and efficient method for direct cloning of PCR products using ddT-tailed vectors. Nucleic Acids Res. 1991 Mar 11;19(5):1156–1156. doi: 10.1093/nar/19.5.1156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Jakubczak J. L., Burke W. D., Eickbush T. H. Retrotransposable elements R1 and R2 interrupt the rRNA genes of most insects. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3295–3299. doi: 10.1073/pnas.88.8.3295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Janetzky B., Lehle L. Ty4, a new retrotransposon from Saccharomyces cerevisiae, flanked by tau-elements. J Biol Chem. 1992 Oct 5;267(28):19798–19805. [PubMed] [Google Scholar]
  24. Johnson G. D., Pirtle I. L., Pirtle R. M. The nucleotide sequence of tyrosine tRNAQ* psi A from bovine liver. Arch Biochem Biophys. 1985 Jan;236(1):448–453. doi: 10.1016/0003-9861(85)90647-2. [DOI] [PubMed] [Google Scholar]
  25. Johnson M. S., McClure M. A., Feng D. F., Gray J., Doolittle R. F. Computer analysis of retroviral pol genes: assignment of enzymatic functions to specific sequences and homologies with nonviral enzymes. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7648–7652. doi: 10.1073/pnas.83.20.7648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Julien J., Poirier-Hamon S., Brygoo Y. Foret1, a reverse transcriptase-like sequence in the filamentous fungus Fusarium oxysporum. Nucleic Acids Res. 1992 Aug 11;20(15):3933–3937. doi: 10.1093/nar/20.15.3933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lecanidou R., Eickbush T. H., Kafatos F. C. Ribosomal DNA genes of Bombyx mori: a minor fraction of the repeating units contain insertions. Nucleic Acids Res. 1984 Jun 11;12(11):4703–4713. doi: 10.1093/nar/12.11.4703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Levin H. L., Weaver D. C., Boeke J. D. Two related families of retrotransposons from Schizosaccharomyces pombe. Mol Cell Biol. 1990 Dec;10(12):6791–6798. doi: 10.1128/mcb.10.12.6791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lucas H., Moore G., Murphy G., Flavell R. B. Inverted repeats in the long-terminal repeats of the wheat retrotransposon Wis 2-1A. Mol Biol Evol. 1992 Jul;9(4):716–728. doi: 10.1093/oxfordjournals.molbev.a040742. [DOI] [PubMed] [Google Scholar]
  30. Marlor R. L., Parkhurst S. M., Corces V. G. The Drosophila melanogaster gypsy transposable element encodes putative gene products homologous to retroviral proteins. Mol Cell Biol. 1986 Apr;6(4):1129–1134. doi: 10.1128/mcb.6.4.1129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. McClure M. A. Evolution of retroposons by acquisition or deletion of retrovirus-like genes. Mol Biol Evol. 1991 Nov;8(6):835–856. doi: 10.1093/oxfordjournals.molbev.a040686. [DOI] [PubMed] [Google Scholar]
  32. McHale M. T., Roberts I. N., Noble S. M., Beaumont C., Whitehead M. P., Seth D., Oliver R. P. CfT-I: an LTR-retrotransposon in Cladosporium fulvum, a fungal pathogen of tomato. Mol Gen Genet. 1992 Jun;233(3):337–347. doi: 10.1007/BF00265429. [DOI] [PubMed] [Google Scholar]
  33. Michaille J. J., Mathavan S., Gaillard J., Garel A. The complete sequence of mag, a new retrotransposon in Bombyx mori. Nucleic Acids Res. 1990 Feb 11;18(3):674–674. doi: 10.1093/nar/18.3.674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Mount S. M., Rubin G. M. Complete nucleotide sequence of the Drosophila transposable element copia: homology between copia and retroviral proteins. Mol Cell Biol. 1985 Jul;5(7):1630–1638. doi: 10.1128/mcb.5.7.1630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Pearl L. H., Taylor W. R. A structural model for the retroviral proteases. Nature. 1987 Sep 24;329(6137):351–354. doi: 10.1038/329351a0. [DOI] [PubMed] [Google Scholar]
  36. Rothnie H. M., McCurrach K. J., Glover L. A., Hardman N. Retrotransposon-like nature of Tp1 elements: implications for the organisation of highly repetitive, hypermethylated DNA in the genome of Physarum polycephalum. Nucleic Acids Res. 1991 Jan 25;19(2):279–286. doi: 10.1093/nar/19.2.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Saigo K., Kugimiya W., Matsuo Y., Inouye S., Yoshioka K., Yuki S. Identification of the coding sequence for a reverse transcriptase-like enzyme in a transposable genetic element in Drosophila melanogaster. Nature. 1984 Dec 13;312(5995):659–661. doi: 10.1038/312659a0. [DOI] [PubMed] [Google Scholar]
  38. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  39. Sandmeyer S. B., Hansen L. J., Chalker D. L. Integration specificity of retrotransposons and retroviruses. Annu Rev Genet. 1990;24:491–518. doi: 10.1146/annurev.ge.24.120190.002423. [DOI] [PubMed] [Google Scholar]
  40. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Schwarz-Sommer Z., Leclercq L., Göbel E., Saedler H. Cin4, an insert altering the structure of the A1 gene in Zea mays, exhibits properties of nonviral retrotransposons. EMBO J. 1987 Dec 20;6(13):3873–3880. doi: 10.1002/j.1460-2075.1987.tb02727.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Smyth D. R., Kalitsis P., Joseph J. L., Sentry J. W. Plant retrotransposon from Lilium henryi is related to Ty3 of yeast and the gypsy group of Drosophila. Proc Natl Acad Sci U S A. 1989 Jul;86(13):5015–5019. doi: 10.1073/pnas.86.13.5015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Springer M. S., Davidson E. H., Britten R. J. Retroviral-like element in a marine invertebrate. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8401–8404. doi: 10.1073/pnas.88.19.8401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Suter B., Altwegg M., Choffat Y., Kubli E. The nucleotide sequence of two homogeneic Drosophila melanogaster tRNATyr isoacceptors: application of a rapid tRNA anticodon sequencing method using S-1 nuclease. Arch Biochem Biophys. 1986 May 15;247(1):233–237. doi: 10.1016/0003-9861(86)90552-7. [DOI] [PubMed] [Google Scholar]
  45. Voytas D. F., Ausubel F. M. A copia-like transposable element family in Arabidopsis thaliana. Nature. 1988 Nov 17;336(6196):242–244. doi: 10.1038/336242a0. [DOI] [PubMed] [Google Scholar]
  46. Weiner A. M., Deininger P. L., Efstratiadis A. Nonviral retroposons: genes, pseudogenes, and transposable elements generated by the reverse flow of genetic information. Annu Rev Biochem. 1986;55:631–661. doi: 10.1146/annurev.bi.55.070186.003215. [DOI] [PubMed] [Google Scholar]
  47. Xiong Y. E., Eickbush T. H. Functional expression of a sequence-specific endonuclease encoded by the retrotransposon R2Bm. Cell. 1988 Oct 21;55(2):235–246. doi: 10.1016/0092-8674(88)90046-3. [DOI] [PubMed] [Google Scholar]
  48. Xiong Y., Burke W. D., Jakubczak J. L., Eickbush T. H. Ribosomal DNA insertion elements R1Bm and R2Bm can transpose in a sequence specific manner to locations outside the 28S genes. Nucleic Acids Res. 1988 Nov 25;16(22):10561–10573. doi: 10.1093/nar/16.22.10561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Xiong Y., Eickbush T. H. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 1990 Oct;9(10):3353–3362. doi: 10.1002/j.1460-2075.1990.tb07536.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Xiong Y., Eickbush T. H. Similarity of reverse transcriptase-like sequences of viruses, transposable elements, and mitochondrial introns. Mol Biol Evol. 1988 Nov;5(6):675–690. doi: 10.1093/oxfordjournals.molbev.a040521. [DOI] [PubMed] [Google Scholar]
  51. Xiong Y., Eickbush T. H. The site-specific ribosomal DNA insertion element R1Bm belongs to a class of non-long-terminal-repeat retrotransposons. Mol Cell Biol. 1988 Jan;8(1):114–123. doi: 10.1128/mcb.8.1.114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Yue X. N., Sakaguchi B., Eickbush T. H. Gene conversions can generate sequence variants in the late chorion multigene families of Bombyx mori. Genetics. 1988 Sep;120(1):221–231. doi: 10.1093/genetics/120.1.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Yuki S., Inouye S., Ishimaru S., Saigo K. Nucleotide sequence characterization of a Drosophila retrotransposon, 412. Eur J Biochem. 1986 Jul 15;158(2):403–410. doi: 10.1111/j.1432-1033.1986.tb09767.x. [DOI] [PubMed] [Google Scholar]
  54. de Chastonay Y., Felder H., Link C., Aeby P., Tobler H., Müller F. Unusual features of the retroid element PAT from the nematode Panagrellus redivivus. Nucleic Acids Res. 1992 Apr 11;20(7):1623–1628. doi: 10.1093/nar/20.7.1623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. van Tol H., Stange N., Gross H. J., Beier H. A human and a plant intron-containing tRNATyr gene are both transcribed in a HeLa cell extract but spliced along different pathways. EMBO J. 1987 Jan;6(1):35–41. doi: 10.1002/j.1460-2075.1987.tb04715.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES