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Genomic expansion of the Bov-A2 retroposon relating to phylogeny and breed management

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Abstract

Bov-A2 is a retroposon that is widely distributed among the genomes of ruminants (e.g., cow, deer, giraffe, pronghorn, musk deer, and chevrotain). This retroposon is composed of two monomers, called Bov-A units, which are joined by a linker sequence. The structure and origin of Bov-A2 has been well characterized but a genome-level exploration of this retroposon has not been implemented. In this study we performed an extensive search for Bov-A2 using all available genome sequence data on Bos taurus. We found unique Bov-A2-derived sequences that were longer than Bov-A2 due to amplification of three to six Bov-A units arranged in tandem. Detailed analysis of these elongated Bov-A2-derived sequences revealed that they originated through unequal crossing-over of Bov-A2. We found a large number of these elongated Bov-A2-derived sequences in cattle genomes, indicating that unequal crossing-over of Bov-A2 occurred very frequently. We found that this type of elongation is not observed in wild bovine and is therefore specific to the domesticated cattle genome. Furthermore, at specific loci, the number of Bov-A units was also polymorphic between alleles, implying that the elongation of Bov-A units might have occurred very recently. For these reasons, we speculate that genomic instability in bovine genomes can lead to extensive unequal crossing-over of Bov-A2 and levels of polymorphism might be generated in part by repeated outbreeding.

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References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Band M, Ron M (1994) Isolation of polymorphic AGC repeats located 3′ to bovine SINEs. Anim Genet 25, 281–283

    Article  PubMed  CAS  Google Scholar 

  • Band M, Ron M (1996) Creation of a SINE enriched library for the isolation of polymorphic (AGC)n microsatellite markers in the bovine genome. Anim Genet 27, 243–248

    Article  PubMed  CAS  Google Scholar 

  • Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL (2005) GenBank. Nucleic Acids Res 33, D34–D38

    Article  PubMed  CAS  Google Scholar 

  • Blin N, Stafford DW (1976) A general method for isolation of high molecular weight DNA from eukaryotes. Nucleic Acids Res 3, 2303–2308

    PubMed  CAS  Google Scholar 

  • Bois PR (2003) Hypermutable minisatellites, a human affair? Genomics 81, 349–355

    Article  PubMed  CAS  Google Scholar 

  • Bruford MW, Bradley DG, Luikart G (2003) DNA markers reveal the complexity of livestock domestication. Nat Rev Genet 4, 900–910

    Article  PubMed  CAS  Google Scholar 

  • Damiani G, Florio S, Budelli E, Bolla P, Caroli A (2000) Single nucleotide polymorphisms (SNPs) within Bov-A2 SINE in the second intron of bovine and buffalo k-casein (CSN3) gene. Anim Genet 31, 277–279

    Article  PubMed  CAS  Google Scholar 

  • Gatesy J, Yelon D, DeSalle R, Vrba ES (1992) Phylogeny of the Bovidae (Artiodactyla, Mammalia), based on mitochondrial ribosomal DNA sequences. Mol Biol Evol 9, 433–446

    PubMed  CAS  Google Scholar 

  • Groves P, Shields GF (1996) Phylogenetics of the Caprinae based on cytochrome b sequence. Mol Phylogenet Evol 5, 467–476

    Article  PubMed  CAS  Google Scholar 

  • Hassanin A, Douzery EJ (1999) The tribal radiation of the family Bovidae (Artiodactyla) and the evolution of the mitochondrial cytochrome b gene. Mol Phylogenet Evol 13, 227–243

    Article  PubMed  CAS  Google Scholar 

  • Hassanin A, Douzery EJ (2003) Molecular and morphological phylogenies of ruminantia and the alternative position of the moschidae. Syst Biol 52, 206–228

    Article  PubMed  Google Scholar 

  • Hassanin A, Ropiquet A (2004) Molecular phylogeny of the tribe Bovini (Bovidae, Bovinae) and the taxonomic status of the Kouprey, Bos sauveli Urbain 1937. Mol Phylogenet Evol 33, 896–907

    Article  PubMed  CAS  Google Scholar 

  • Hassanin A, Ropiquet A, Cornette R, Tranier M, Pfeffer P, et al. (2006) Has the kouprey (Bos sauveli Urbain, 1937) been domesticated in Cambodia? C R Biol 329, 124–135

    PubMed  Google Scholar 

  • Hawken RJ, Barris WC, McWilliam SM, Dalrymple BP (2004) An interactive bovine in silico SNP database (IBISS). Mamm Genome 15, 819–827

    Article  PubMed  CAS  Google Scholar 

  • Jobse C, Buntjer JB, Haagsma N, Breukelman HJ, Beintema JJ, et al. (1995) Evolution and recombination of bovine DNA repeats. J Mol Evol 41, 277–283

    Article  PubMed  CAS  Google Scholar 

  • Kaukinen J, Varvio SL (1992) Artiodactyl retroposons: association with microsatellites and use in SINEmorph detection by PCR. Nucleic Acids Res 20, 2955–2958

    Article  PubMed  CAS  Google Scholar 

  • Lenstra JA, van Boxtel JAF, Zwaaagstra KA, Schwerin M (1993) Short interspersed nuclear element (SINE) sequences of the Bovidae. Anim Genet 24, 33–39

    Article  PubMed  CAS  Google Scholar 

  • Lipman DJ, Pearson WR (1985) Rapid and sensitive protein similarity searches. Science 227, 1435–1441

    Article  PubMed  CAS  Google Scholar 

  • Lum JK, Nikaido M, Shimamura M, Shimodaira H, Shedlock AM, et al. (2000) Consistency of SINE insertion topology and flanking sequence tree: quantifying relationships among cetartiodactyls. Mol Biol Evol 17, 1417–1424

    PubMed  CAS  Google Scholar 

  • Mannen H, Tsuji S, Loftus RT, Bradley DG (1998) Mitochondrial DNA variation and evolution of Japanese black cattle (Bos taurus). Genetics 150, 1169–1175

    PubMed  CAS  Google Scholar 

  • Namikawa T, Widodo W (1978) Electrophoretic variations of hemoglobin and serum albumin in the Indonesian cattle including Bali cattle (Bos banteng). Jpn J Zootech Sci 49, 817–827

    CAS  Google Scholar 

  • Nijman IJ, van Tessel P, Lenstra JA (2002) SINE retrotransposon during the evolution of the pecoran ruminants. J Mol Evol 54, 9–16

    Article  PubMed  CAS  Google Scholar 

  • Nijman IJ, Otsen M, Verkaar EL, de Ruijter C, Hanekamp E, et al. (2003) Hybridization of banteng (Bos javanicus) and zebu (Bos indicus) revealed by mitochondrial DNA, satellite DNA, AFLP and microsatellites. Heredity 90, 10–16

    Article  PubMed  CAS  Google Scholar 

  • Ogawa Y, Daigo M, Amasaki H (1989) Craniometrical estimation of the native Japanese Mishima cattle, using multivariate analysis. Anat Anz 168, 197–202

    PubMed  CAS  Google Scholar 

  • Ohshima K, Hamada M, Terai Y, Okada N (1996) The 3′ ends of tRNA-derived short interspersed repetitive elements are derived from the 3′ ends of long interspersed repetitive elements. Mol Cell Biol 16, 3756–3764

    PubMed  CAS  Google Scholar 

  • Okada N, Hamada M (1997) The 3′ ends of tRNA-derived SINEs originated from the 3′ ends of LINEs: a new example from the bovine genome. J Mol Evol 44, S52–S56

    Article  PubMed  CAS  Google Scholar 

  • Rogers JH (1985) The origin and evolution of retroposons. Int Rev Cytol 93, 187–179

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto K, Okada N (1985) Rodent type 2 Alu family, rat identifier sequence, rabbit C family, and bovine or goat 73-bp repeat may have evolved from tRNA genes. J Mol Evol 22, 134–140

    Article  PubMed  CAS  Google Scholar 

  • Sasazaki S, Lee JE, Mannen H, Kunieda T, Sakurai T, et al. (2001) Phylogenetic analysis of five beef cattle breeds using AFLP marker. Anim Sci J 72, J1–J5

    CAS  Google Scholar 

  • Schmidt P, Kuhn C, Maillard JC, Pitra C, Tiemann U, et al. (2002) A comprehensive survey for polymorphisms in the bovine IFN-gamma gene reveals a highly polymorphic intronic DNA sequence allowing improved genotyping of Bovinae. J Interferon Cytokine Res 22, 923–934

    Article  PubMed  CAS  Google Scholar 

  • Shedlock AM, Okada N (2000) SINE insertions: powerful tools for molecular systematics. Bioessays 22, 148–160

    Article  PubMed  CAS  Google Scholar 

  • Shimamura M, Yasue H, Ohshima K, Abe H, Kato H, et al. (1997) Molecular evidence from retroposons that whales form a clade within even-toed ungulates. Nature 388, 666–670

    Article  PubMed  CAS  Google Scholar 

  • Shimamura M, Abe H, Nikaido M, Ohshima K, Okada N (1999) Genealogy of families of SINEs in cetaceans and artiodactyls: the presence of a huge superfamily of tRNA(Glu)-derived families of SINEs. Mol Biol Evol 16, 1046–1060

    PubMed  CAS  Google Scholar 

  • Singer MF (1982) SINEs and LINEs: highly repeated short and long interspersed sequences in mammalian genomes. Cell 28, 433–434

    Article  PubMed  CAS  Google Scholar 

  • Singer M, Berg P (1991) Genes and Genomes. (Mill Valley, CA: University Science Books)

    Google Scholar 

  • Szemraj J, Plucienniczak G, Jaworski J, Plucienniczak A (1995) Bovine Alu-like sequences mediate transposition of a new site-specific retroelement. Gene 152, 261–264

    Article  PubMed  CAS  Google Scholar 

  • Tajima K, Enishi O, Amari M, Mitsumori M, Kajikawa H, et al. (2002) PCR detection of DNAs of animal origin in feed by primers based on sequences of short and long interspersed repetitive elements. Biosci Biotechnol Biochem 66, 2247–2250

    Article  PubMed  CAS  Google Scholar 

  • Troy CS, MacHugh DE, Bailey JF, Magee DA, Loftus RT, et al. (2001) Genetic evidence for Near-Eastern origins of European cattle. Nature 410, 1088–1091

    Article  PubMed  CAS  Google Scholar 

  • Vila C, Seddon J, Ellegren H (2005) Genes of domestic mammals augmented by backcrossing with wild ancestors. Trends Genet 21, 214–218

    Article  PubMed  CAS  Google Scholar 

  • Walker JA, Hughes DA, Anders BA, Shewale J, Sinha SK, et al. (2003) Quantitative intra-short interspersed element PCR for species-specific DNA identification. Anal Biochem 316, 259–269

    Article  PubMed  CAS  Google Scholar 

  • Weiner AM, Deininger PL, Efstratiadis A (1986) Nonviral retroposons: genes, pseudogenes, and transposable elements generated by the reverse flow of genetic information. Annu Rev Biochem 55, 631–661

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank the following individuals and organizations for providing samples: Dr. H. Taru (Kanagawa Prefectural Museum of Natural History, Kanagawa); Dr. I. Munechika (Chiba Zoological Park, Chiba); Meat Inspection Station, Kanagawa Prefectural Government (Kanagawa); Ueno Zoological Gardens (Tokyo); and Zoological Society of San Diego’s Center for Reproduction of Endangered Species (San Diego). The authors especially appreciate the support of and discussion with Dr. M. Hasegawa (Department of Biosystems Science, The Graduate University for Advanced Studies, and The Institute of Statistical Mathematics). This work was supported by a Grant-in-Aid to NO from the Ministry of Education, Science, Sports and Culture of Japan.

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Authors and Affiliations

  1. Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama, Japan

    Jun-ichi Onami, Masato Nikaido & Norihiro Okada

  2. Faculty of Agriculture, Kobe University, Kobe, Japan

    Hideyuki Mannen

  3. Department of Speciation, National Institute for Basic Biology, Okazaki, Japan

    Norihiro Okada

  4. Department of Biological Sciences, Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, 4259-B21 Nagatsuta-cho, Midori-ku, Yokohama, 226-8501, Japan

    Norihiro Okada

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  1. Jun-ichi Onami
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  2. Masato Nikaido
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  4. Norihiro Okada
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Correspondence to Norihiro Okada.

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Onami, Ji., Nikaido, M., Mannen, H. et al. Genomic expansion of the Bov-A2 retroposon relating to phylogeny and breed management. Mamm Genome 18, 187–196 (2007). https://doi.org/10.1007/s00335-007-9000-1

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  • DOI: https://doi.org/10.1007/s00335-007-9000-1

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