Skip to main content
Log in

Evolutionary implications of multiple SINE insertions in an intronic region from diverse mammals

  • Original Contributions
  • Published:
Mammalian Genome Aims and scope Submit manuscript

Abstract

An analysis of the nuclear β-fibrinogen intron 7 locus from 30 taxa representing 12 placental orders of mammals reveals the enriched occurrences of short interspersed element (SINE) insertion events. Mammalian-wide interspersed repeats (MIRs) are present at orthologous sites of all examined species except those in the order Rodentia. The higher substitution rate in mouse and a rare MIR deletion from rat account for the absence of MIR in the rodents. A minimum of five lineage-specific SINE sequences are also found to have independently inserted into this intron in Carnivora, Artiodactyla and Lagomorpha. In the case of Carnivora, the unique amplification pattern of order-specific CAN SINE provides important evidence for the “pan-carnivore” hypothesis of this repeat element and reveals that the CAN SINE family may still be active today. Particularly interesting is the finding that all identified lineage-specific SINE elements show a strong tendency to insert within or in very close proximity to the preexisting MIRs for their efficient integrations, suggesting that the MIR element is a hot spot for successive insertions of other SINEs. The unexpected MIR excision as a result of a random deletion in the rat intron locus and the non-random site targeting detected by this study indicate that SINEs actually have a greater insertional flexibility and regional specificity than had previously been recognized. Implications for SINE sequence evolution upon and following integration, as well as the fascinating interactions between retroposons and the host genomes are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

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

    Article  PubMed  Google Scholar 

  • Batzer MA, Deininger PL (2002) Alu repeats and human genomic diversity. Nature Reviews Genetics 3: 370–379

    Article  PubMed  Google Scholar 

  • Betley JN, Frith MC, Graber JH, Choo S, Deshler JO (2002) A ubiquitous and conserved signal for RNA localization in chordates. Current Biology 12: 1756–1761

    Article  PubMed  Google Scholar 

  • Cantrell MA, Filanoski BJ, Ingermann AR, Olsson K, DiLuglio N, Lister Z, Wichman HA (2001) An ancient retrovirus-like element contains hot spots for SINE insertion. Genetics 158: 769–777

    PubMed  Google Scholar 

  • Coltman DW, Wright JM (1994) Can SINEs: a family of tRNA-derived retroposons specific to the superfamily Canoidea. Nucleic Acids Research 22: 2726–2730

    PubMed  Google Scholar 

  • Das M, Chu LL, Ghahremani M, Abrams-Ogg T, Roy MS, Housman D, Pelletier J (1998) Characterization of an abundant short interspersed nuclear element (SINE) present in Canis familiaris. Mamm Genome 9: 64–69

    Article  PubMed  Google Scholar 

  • Deininger PL (1989) SINEs: short interspersed repeated DNA elements in higher eukaryotes. In: Berg DE, Howe MM (Eds.), Mobile DNA. American Society of Microbiology, Washington DC, pp. 619–636

    Google Scholar 

  • Deininger PL, Moran JV, Batzer MA, Kazazian Jr HH (2003) Mobile elements and mammalian genome evolution. Current Opinion in Genetics and Development 13: 651–658

    Article  PubMed  Google Scholar 

  • Doolittle RF (1984) Fibrinogen and fibrin. Ann Rev Biochem 53: 195–229

    PubMed  Google Scholar 

  • Edwards MC, Gibbs RA (1992) A human dimorphism resulting from loss of an Alu. Genomics 14: 590–597

    Article  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783–791

    Google Scholar 

  • Frengen E, Thomsen P, Kristensen T, Kran S, Miller R, Davies W (1991) Porcine SINEs: characterization and use in species-specific amplification. Genomics 10: 949–956

    Article  PubMed  Google Scholar 

  • Gilbert N, Labuda D (1999) CORE-SINEs: eukaryotic short interspersed retroposing elements with common sequence motifs. Proc Natl Acad Sci USA 96: 2869–2874

    Article  PubMed  Google Scholar 

  • Gilbert N, Labuda D (2000) Evolutionary inventions and continuity of CORE-SINEs in Mammals. J Mol Biol 298: 365–377

    Article  PubMed  Google Scholar 

  • Hughes DC (2000) MIRs as agents of mammalian gene evolution. Trends in Genetics 16: 60–62

    Google Scholar 

  • Jurka J, Zietkiewicz E, Labuda D (1995) Ubiquitous mammalian-wide interspersed repeats (MIRs) are molecular fossils from the Mesozoic era. Nucl Acids Res 23: 170–175

    PubMed  Google Scholar 

  • Jurka J, Klonowski P (1996) Integration of retroposable elements in mammals: selection of target sites. J Mol Evol 43: 685–689

    Article  PubMed  Google Scholar 

  • Jurka J, Klonowski P, Trifnonv EN (1998) Mammalian retroposons integrate at kinkable DNA sites. J Biomol Struct Dyn 15: 717–721

    PubMed  Google Scholar 

  • Kidwell MG, Lisch DR (2001) Perspective: transposable elements, parasitic DNA, and genome evolution. Evolution 55: 1–24

    PubMed  Google Scholar 

  • Krane DE, Clark AG, Cheng JF, Hardison RC (1991) Subfamily relationships and clustering of rabbit C repeats. Mol Biol Evol 8: 1–30

    PubMed  Google Scholar 

  • Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: Molecular Evolutionary Genetics Analysis Software. Version 2.1. (Tempe, Arizona, USA: Arizona State University)

  • Maraia RJ (1995) The impact of short interspersed elements (SINEs) on the host genome. Springer-Verlag, New York

    Google Scholar 

  • Minnick MF, Stillwell LC, Heinerman JM, Stiegler GL (1992) A highly repetitive DNA sequence possibly unique to canids. Gene 110: 235–238

    Article  PubMed  Google Scholar 

  • Nikaido M, Matsuno F, Hamilton H, Brownell RL, Cao Y, Ding W, Zuoyan Z, Shedlock AW, Fordyce RE, Hasegawa M, Okada N (2001) Retroposon analysis of major cetacean lineages:The monophyly of toothed whales and the paraphyly of river dolphins. Proc Natl Acad Sci USA 98: 7384–7389

    Article  PubMed  Google Scholar 

  • Okada N (1991) SINEs: short interspersed repeated elements of the eukaryotic genome. Trends Ecol Evol 6: 358–361

    Article  Google Scholar 

  • Pecon Slattery J, Murphy WJ, O’Brien SJ (2000) Patterns of diversity among SINE elements isolated from three Y-chromosome genes in carnivores. Mol Biol Evol 17: 825–829

    PubMed  Google Scholar 

  • Qin ZH, Schuller I, Richter G, Diamantstein T, Blankenstein T (1991) The interleukin- 6 gene locus seems to be a preferred target site for retrotransposons and retroviruses. Immunogenetics 33: 260–266

    Article  PubMed  Google Scholar 

  • Rogers JH (1985) The origin and evolution of retroposons. Int Rev Cytol 93: 187–279

    PubMed  Google Scholar 

  • Salem AH, Ray DA, Xing JC, Callinan PA, Myers JS, Hedges DJ, Garber PK, Witherspoon DJ, Jorde LB, Batzer MA (2003) Alu elements and hominid phylogenetics. Proc Natl Acad Sci USA 100: 12787–12791

    Article  PubMed  Google Scholar 

  • Sambrook E, Fritsch F, Maniatis T (1989) Molecular Clonging. Cold Spring Harbor Press, Cold Spring Harbor, NY

    Google Scholar 

  • Schiefelbein JW, Furtek DB, Dooner HK, Nelson Jr OE (1988) Two mutations in a maize bronze-1 allele caused by transposable elements of the Ac-Ds family alter the quantity and quality of the gene product. Genetics 120: 767–777

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Slagel V, Flemington E, Traina-Dorge V, Bradshaw H, Deininger P (1987) Clustering and subfamily relationships of the Alu family in the human genome. Mol Biol Evol 4: 19–29

    PubMed  Google Scholar 

  • Smit AF, Riggs AD (1995) MIRs are classic, tRNA-derived SINEs that amplified before the mammalian radiation. Nucleic Acids Res 23: 98–102

    PubMed  Google Scholar 

  • Tatout C, Lavie L, Deragon JM (1998) Similar target site selection occurs in integration of plant and mammalian retroposons. J Mol Evol 47: 463–470

    PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. (1997) The clustalx windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24: 4876–4882

    Article  Google Scholar 

  • Van der Vlugt HH, Lenstra JA (1995) SINE elements of carnivores. Mamm Genome 6: 49–51

    Article  PubMed  Google Scholar 

  • Vassetzky NS, Kramerov DA (2002) CAN—a pan-carnivore SINE family. Mamm Genome 13: 50–57

    Article  PubMed  Google Scholar 

  • Wang TH, Johnson N, Zou J, Bols N, Secombes CH (2004) Sequencing and expression of the second allele of the interleukin-1β1 gene in rainbow trout (Oncorhynchus mykiss): identification of a novel SINE in the third intron. Fish & Shellfish Immunology 16: 335–358

    Google Scholar 

  • Wells D, Bains W (1991) Characterization of an unusual human histone H3.3 pseudogene. DNA Seq 2: 125–127

    PubMed  Google Scholar 

  • Wessler SR (1988) Phenotypic diversity mediated by the maize transposable elements Ac and Spm. Science 242: 399-405

    PubMed  Google Scholar 

  • Wichman HA, Van Den Bussche RA, Hamilton MJ, Baker RJ (1992) Transposable elements and the evolution of genome organization in mammals. Genetica 86: 287–293

    Article  PubMed  Google Scholar 

  • Yu L, Zhang YP (2004) Phylogenetic studies of pantherine cats (Felidae) based on multiple genes, with novel application of nuclear β-Fibrinogen intron 7 to carnivores. Mol Phylogenet Evol 35: 483–495

    Article  Google Scholar 

  • Zehr SM, Nedbal MA, Flynn JJ (2001) Tempo and mode of evolution in an orthologous Can SINE. Mamm Genome 12: 38–44

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the grants from National Natural Science Foundation of China (NSFC) and Chinese Academy of Science. Additionally, we thank Dr. Alfred Roca, Dr. Warren Johnson and Ms. Luo Shujin, National Cancer Institute, Laboratory of Genomic Diversity for improving the English of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ya-ping Zhang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yu, L., Zhang, Yp. Evolutionary implications of multiple SINE insertions in an intronic region from diverse mammals. Mamm Genome 16, 651–660 (2005). https://doi.org/10.1007/s00335-004-2456-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00335-004-2456-3

Keywords

Navigation