Genes & Genomics

, Volume 35, Issue 4, pp 483–489 | Cite as

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

  • Kung Ahn
  • Jin-Han Bae
  • Jeong-An Gim
  • Ja-Rang Lee
  • Yi-Deun Jung
  • Kyung-Do Park
  • Kyudong Han
  • Byung-Wook Cho
  • Heui-Soo Kim
Research Article

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

Horse Transposable elements (TEs) Retroelements DNA elements 

Supplementary material

13258_2013_57_MOESM1_ESM.ppt (138 kb)
Supplementary Fig. 1. Confidence Interval for Insertional Orientation of Transposable Elements in the Horse Genome. In this study, a total of 625 sense oriented and 685 antisense oriented TEs were detected in the horse genome. This figure illustrates the expected range in distribution for these 1310 TE insertions assuming equal probability (p = 0.5) of TE insertions occurring in either orientation. As can be seen from the binomial distribution, the number of sense and antisense orientations are consistent with a random TE orientational insertion preference. Supplementary material 1 (PPT 137 kb)

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 41:91–99PubMedCrossRefGoogle Scholar
  2. Baltimore D (1985) Retroviruses and retrotransposons: the role of reverse transcription in shaping the eukaryotic genome. Cell 40:481–482PubMedCrossRefGoogle Scholar
  3. Biémont C, Vieira C (2006) Genetics: junk DNA as an evolutionary force. Nature 443:521–524PubMedCrossRefGoogle Scholar
  4. Bourque G (2009) Transposable elements in gene regulation and in the evolution of vertebrate genomes. Curr Opin Genet Dev 19:607–612PubMedCrossRefGoogle Scholar
  5. Britten RJ (2010) Transposable element insertions have strongly affected human evolution. Proc Natl Acad Sci USA 107:19945–19948PubMedCrossRefGoogle Scholar
  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 4:23–27CrossRefGoogle Scholar
  7. Chen LL, DeCerbo JN, Carmichae GG (2008) Alu element-mediated gene silencing. EMBO J 27:1694–1705PubMedCrossRefGoogle Scholar
  8. Cordaux R, Batzer MA (2009) The impact of retrotransposons on human genome evolution. Nat Rev Genet 10:691–703PubMedCrossRefGoogle Scholar
  9. Curtis D, Lehmann R, Zamore PD (1995) Translational regulation in development. Cell 81:171–178PubMedCrossRefGoogle Scholar
  10. Deragon JM, Capy P (2000) Impact of transposable elements on the human genome. Ann Med 32:264–273PubMedGoogle Scholar
  11. Goodier JL, Kazazian HH Jr (2008) Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 135:23–35PubMedCrossRefGoogle Scholar
  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 3:1939–1949PubMedCrossRefGoogle Scholar
  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 105:19366–19371PubMedCrossRefGoogle Scholar
  14. Jurka J (2000) Repbase update: a database and an electronic journal of repetitive elements. Trends Genet 16:418–420PubMedCrossRefGoogle Scholar
  15. Kazazian HH Jr (2004) Mobile elements: drivers of genome evolution. Science 303:1626–1632PubMedCrossRefGoogle Scholar
  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 7:719Google Scholar
  17. Krane DE, Hardiso RC (1990) Short interspersed repeats in rabbit DNA can provide functional polyadenylation signals. Mol Biol Evol 7:1–8PubMedGoogle Scholar
  18. Krull M, Petrusma M, Makalowski W, Brosius J, Schmitz J (2007) Functional persistence of exonized mammalian-wide interspersed repeat elements (MIRs). Genome Res 17:1139–1145PubMedCrossRefGoogle Scholar
  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 435:29–35PubMedCrossRefGoogle Scholar
  20. Lin L, Jiang P, Shen S, Sato S, Davidson BL, Xing Y (2009) Large-scale analysis of exonized mammalian-wide interspersed repeats in primate genomes. Hum Mol Genet 18:2204–2214PubMedCrossRefGoogle Scholar
  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 76:2410–2423PubMedCrossRefGoogle Scholar
  22. Lithgow T, Cuezvab J, Silverc PA (1997) Highways for protein delivery to the mitochondria. Trends Biochem Sci 22:110–113PubMedCrossRefGoogle Scholar
  23. Lorenc A, Makałowsk W (2003) Transposable elements and vertebrate protein diversity. Genetica 118:183–191PubMedCrossRefGoogle Scholar
  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 276:1896–1903PubMedCrossRefGoogle Scholar
  25. Moran JV, Malik HS (2009) Diamonds and rust: how transposable elements influence mammalian genomes. EMBO Rep 10:1306–1310PubMedCrossRefGoogle Scholar
  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) 5′-RACE cDNA library. Anim Genet 33:231–232PubMedCrossRefGoogle Scholar
  27. Reiss D, Zhang Y, Mager DL (2007) Widely variable endogenous retroviral methylation levels in human placenta. Nucleic Acids Res 35:4743–4754PubMedCrossRefGoogle Scholar
  28. Robertson HM (2002) In: Craig NL et al (eds) Mobile DNA II, Evolution of DNA transposons in eukaryotes. ASM Press, Washington, DC, pp 1093–1110Google Scholar
  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:R59PubMedCrossRefGoogle Scholar
  30. Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8:272–285PubMedCrossRefGoogle Scholar
  31. Smalheiser NR, Torvik VI (2005) Mammalian microRNAs derived from genomic repeats. Trends Genet 21:322–326PubMedCrossRefGoogle Scholar
  32. Ting CN, Rosenberg MP, Snow CM, Samuelson LC, Meisler MH (1992) Endogenous retroviral sequences are required for tissue-specific expression of a human salivary amylase gene. Genes Dev 6:1457–1465PubMedCrossRefGoogle Scholar
  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 19:530–536PubMedCrossRefGoogle Scholar
  34. Varagona MJ, Purugganan M, Wessle SR (1992) Alternative splicing induced by insertion of retrotransposons into the maize waxy gene. Plant Cell 4:811–820PubMedGoogle Scholar
  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 326:865–867PubMedCrossRefGoogle Scholar
  36. Wu J, Grindlay GJ, Bushel P, Mendelsohn L, Allan M (1990) Negative regulation of the human epsilon-globin gene by transcriptional interference: role of an Alu repetitive element. Mol Cell Biol 10:1209–1216PubMedGoogle Scholar

Copyright information

© The Genetics Society of Korea 2013

Authors and Affiliations

  • Kung Ahn
    • 1
  • Jin-Han Bae
    • 1
  • Jeong-An Gim
    • 1
  • Ja-Rang Lee
    • 1
  • Yi-Deun Jung
    • 1
  • Kyung-Do Park
    • 2
  • Kyudong Han
    • 3
  • Byung-Wook Cho
    • 4
  • Heui-Soo Kim
    • 1
  1. 1.Department of Biological SciencesCollege of Natural Sciences, Pusan National UniversityPusanRepublic of Korea
  2. 2.Department of Animal Life and Environment SciencesHankyong National UniversityAnseongRepublic of Korea
  3. 3.Department of Nanobiomedical Science & WCU Research CenterDankook UniversityCheonanRepublic of Korea
  4. 4.Department of Animal Science, College of Life SciencesPusan National UniversityMiryangRepublic of Korea

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