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Identification and characterization of transposable elements inserted into the coding sequences of horse genes

  • Ahn, Kung (Department of Biological Sciences, College of Natural Sciences, Pusan National University) ;
  • Bae, Jin-Han (Department of Biological Sciences, College of Natural Sciences, Pusan National University) ;
  • Gim, Jeong-An (Department of Biological Sciences, College of Natural Sciences, Pusan National University) ;
  • Lee, Ja-Rang (Department of Biological Sciences, College of Natural Sciences, Pusan National University) ;
  • Jung, Yi-Deun (Department of Biological Sciences, College of Natural Sciences, Pusan National University) ;
  • Park, Kyung-Do (Department of Animal Life and Environment Sciences, Hankyong National University) ;
  • Han, Kyudong (Department of Nanobiomedical Science & WCU Research Center, Dankook University) ;
  • Cho, Byung-Wook (Department of Animal Science, College of Life Sciences, Pusan National University) ;
  • Kim, Heui-Soo (Department of Biological Sciences, College of Natural Sciences, Pusan National University)
  • Published : 2013.08.31

Abstract

Transposable elements (TEs) are repetitive sequences dispersed throughout mammalian genomes, and they occupy important genetic positions. TEs have been shown to have both harmful and beneficial effects such as exonization, polyadenylation, and/or altering transcription rates in various vertebrate genomes. However, to the best of our knowledge, no study has yet considered the relationship between TEs and horse genes. In this study, we examined the contribution of TEs to the horse genome by collecting TEs inserted within mRNA genes. By screening the abundance, distribution, and orientation of TEs, we found that the majority of TE insertions belong to retroelements and DNA elements, most of which exist in the coding sequences of horse genes. In addition, the MIR, L1, L2, ERVL, and ERVL-MaLR subfamilies were found to be the most abundant in both non-LTR and LTR elements. Retroelements (LTRs, LINEs, and SINEs) among the TEs inserted in the coding sequences showed a preference for antisense orientation. The most pronounced imbalance in insertional orientation was observed in LINEs, which represent 40 % of all TEs in antisense orientation. Through these analyses, we identified that a total of 1310 TEs have been integrated into horse mRNA genes and small fractions of them have been exonized into coding sequences.

Keywords

References

  1. Adelson DL, Raison JM, Garber M, Edgar RC (2010) Interspersed repeats in the horse (Equus caballus); spatial correlations highlight conserved chromosomal domains. Anim Genet 41:91-99 https://doi.org/10.1111/j.1365-2052.2010.02115.x
  2. Baltimore D (1985) Retroviruses and retrotransposons: the role of reverse transcription in shaping the eukaryotic genome. Cell 40:481-482 https://doi.org/10.1016/0092-8674(85)90190-4
  3. Biemont C, Vieira C (2006) Genetics: junk DNA as an evolutionary force. Nature 443:521-524 https://doi.org/10.1038/443521a
  4. Bourque G (2009) Transposable elements in gene regulation and in the evolution of vertebrate genomes. CurrOpin Genet Dev 19:607-612 https://doi.org/10.1016/j.gde.2009.10.013
  5. Britten RJ (2010)Transposable element insertions have strongly affected human evolution. Proc Natl Acad Sci USA 107:19945-19948 https://doi.org/10.1073/pnas.1014330107
  6. Capomaccio S, Verini-Supplizi A, Galla G, Vitulo N, Barcaccia G, Felicetti M, Silvestrelli M, Cappelli K (2010) Transcription of LINE-derived sequences in exercise-induced stress in horses. Anim Genet 4:23-27
  7. Chen LL, DeCerbo JN, Carmichae GG (2008) Alu element-mediated gene silencing. EMBO J 27:1694-1705 https://doi.org/10.1038/emboj.2008.94
  8. Cordaux R, Batzer MA (2009) The impact of retrotransposons on human genome evolution. Nat Rev Genet 10:691-703 https://doi.org/10.1038/nrg2640
  9. Curtis D, Lehmann R, Zamore PD (1995) Translational regulation in development. Cell 81:171-178 https://doi.org/10.1016/0092-8674(95)90325-9
  10. Deragon JM, Capy P (2000) Impact of transposable elements on the human genome. Ann Med 32:264-273 https://doi.org/10.3109/07853890009011771
  11. Goodier JL, Kazazian HH Jr (2008) Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 135:23-35 https://doi.org/10.1016/j.cell.2008.09.022
  12. Han K, Lee J, Meyer TJ, Wang J, Sen SK, Srikanta D, Liang P, Batzer MA (2007) Alu recombination-mediated structural deletions in the Chimpanzee Genome. PLoS Genet 3:1939-1949
  13. Han K, Lee J, Meyer TJ, Remedios P, Goodwin L, Batzer MA (2008) L1 recombination-associated deletions generate human genomic variation. Proc Natl Acad Sci USA 105:19366-19371 https://doi.org/10.1073/pnas.0807866105
  14. Jurka J (2000) Repbase update: a database and an electronic journal of repetitive elements. Trends Genet 16:418-420 https://doi.org/10.1016/S0168-9525(00)02093-X
  15. Kazazian HH Jr (2004) Mobile elements: drivers of genome evolution. Science 303:1626-1632 https://doi.org/10.1126/science.1089670
  16. Kim DS, Kim TH, Huh JW, Kim IC, Kim SW, Park HS, Kim HS (2006) Line fusion genes: a database of LINE expression in human genes. BMC Genomics 7:719
  17. Krane DE, Hardiso RC (1990) Short interspersed repeats in rabbit DNA can provide functional polyadenylation signals. Mol Biol Evol 7:1-8
  18. Krull M, Petrusma M, Makalowski W, Brosius J, Schmitz J (2007) Functional persistence of exonized mammalian-wide interspersed repeat elements (MIRs). Genome Res 17:1139-1145 https://doi.org/10.1101/gr.6320607
  19. Lee JR, Huh JW, Kim DS, Ha HS, Ahn K, Kim YJ, Chang KT, Kim HS (2009) Lineage specific evolutionary events on SFTPB gene: alu recombination-mediated deletion (ARMD), exonization, and alternative splicing events. Gene 435:29-35 https://doi.org/10.1016/j.gene.2009.01.008
  20. Lin L, Jiang P, Shen S, Sato S, Davidson BL, Xing Y (2009) Largescale analysis of exonized mammalian-wide interspersed repeats in primate genomes. Hum Mol Genet 18:2204-2214 https://doi.org/10.1093/hmg/ddp152
  21. Ling J, Pi W, Bollag R, Zeng S, Keskintepe M, Saliman H, Krantz S, Whitney B, Tuan D (2002) The solitary long terminal repeats of ERV-9 endogenous retrovirus are conserved during primate evolution and possess enhancer activities in embryonic and hematopoietic cells. J Virol 76:2410-2423 https://doi.org/10.1128/jvi.76.5.2410-2423.2002
  22. Lithgow T, Cuezvab J, Silverc PA (1997) Highways for protein delivery to the mitochondria. Trends Biochem Sci 22:110-113 https://doi.org/10.1016/S0968-0004(97)01007-4
  23. Lorenc A, Makalowsk W (2003) Transposable elements and vertebrate protein diversity. Genetica 118:183-191 https://doi.org/10.1023/A:1024105726123
  24. Medstrand P, Landry JR, Mager DL (2001) Long terminal repeats are used as alternative promoters for the endothelin B receptor and apolipoprotein C-I genes in humans. J Biol Chem 276:1896-1903 https://doi.org/10.1074/jbc.M006557200
  25. Moran JV, Malik HS (2009) Diamonds and rust: how transposable elements influencemammalian genomes. EMBORep 10:1306-1310
  26. Pascual I, Dhar AK, Fan Y, Paradis MR, Arruga MV, Alcivar-Warren A (2002) Isolation of expressed sequence tags from a Thoroughbred horse (Equus caballus) 50-RACE cDNA library. Anim Genet 33:231-232 https://doi.org/10.1046/j.1365-2052.2002.t01-2-00876.x
  27. Reiss D, Zhang Y, Mager DL (2007) Widely variable endogenous retroviral methylation levels in human placenta. Nucleic Acids Res 35:4743-4754 https://doi.org/10.1093/nar/gkm455
  28. Robertson HM (2002) In: Craig NL et al (eds) Mobile DNA II, Evolution of DNA transposons in eukaryotes. ASM Press, Washington, DC, pp 1093-1110
  29. Sela N, Kim E, Ast G (2010) The role of transposable elements in the evolution of non-mammalian vertebrates and invertebrates. Genome Biol 11:R59 https://doi.org/10.1186/gb-2010-11-6-r59
  30. Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8:272-285
  31. Smalheiser NR, Torvik VI (2005) Mammalian microRNAs derived from genomic repeats. Trends Genet 21:322-326 https://doi.org/10.1016/j.tig.2005.04.008
  32. Ting CN, Rosenberg MP, Snow CM, Samuelson LC, Meisler MH (1992) Endogenous retroviral sequences are required for tissuespecific expression of a human salivary amylase gene. Genes Dev 6:1457-1465 https://doi.org/10.1101/gad.6.8.1457
  33. van de Lagemaat LN, Landry JR, Mager DL, Medstrand P (2003) Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends Genet 19:530-536 https://doi.org/10.1016/j.tig.2003.08.004
  34. Varagona MJ, Purugganan M, Wessle SR (1992) Alternative splicing induced by insertion of retrotransposons into the maize waxy gene. Plant Cell 4:811-820 https://doi.org/10.1105/tpc.4.7.811
  35. Wade CM, Giulotto E, Sigurdsson S, Zoli M, Gnerre S, Imsland F, Lear TL, Adelson DL, Bailey E, Bellone RR et al (2009) Genome sequence, comparative analysis, and population genetics of the domestic horse. Science 326:865-867 https://doi.org/10.1126/science.1178158
  36. Wu J, Grindlay GJ, Bushel P, Mendelsohn L, AllanM(1990) Negative regulation of the human epsilon-globin gene by transcriptional interference: role of an Alu repetitive element. Mol Cell Biol 10:1209-1216 https://doi.org/10.1128/MCB.10.3.1209

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