Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1998 Sep;150(1):345–357. doi: 10.1093/genetics/150.1.345

Molecular evolution of two lineages of L1 (LINE-1) retrotransposons in the california mouse, Peromyscus californicus.

N C Casavant 1, R N Lee 1, A N Sherman 1, H A Wichman 1
PMCID: PMC1460335  PMID: 9725851

Abstract

The large number of L1 [long interspersed elements (LINE)-1] sequences found in the genome is due to the insertion of copies of the retrotransposon over evolutionary time. The majority of copies appear to be replicates of a few active, or "master" templates. A continual replacement of master templates over time gives rise to lineages distinguishable by their own unique set of shared-sequence variants. A previous analysis of L1 sequences in deer mice, Peromyscus maniculatus and P. leucopus, revealed two active L1 lineages, marked by different rates of evolution, whose most recent common ancestor predates the expansion of the Peromyscus species. Here we exploit lineage-specific, shared-sequence variants to reveal a paucity of Lineage 2 sequences in at least one species, P. californicus. The dearth of Lineage 2 copies in P. californicus suggests that Lineage 2 may have been unproductive until after the most recent common ancestor of P. californicus and P. maniculatus. We also show that Lineage 1 appears to have a higher rate of evolution in P. maniculatus relative to either P. californicus or P. leucopus. As a phylogenetic tool, L1 lineage-specific variants support a close affinity between P. californicus and P. eremicus relative to the other species examined.

Full Text

The Full Text of this article is available as a PDF (992.5 KB).

Selected References

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

  1. Adey N. B., Schichman S. A., Graham D. K., Peterson S. N., Edgell M. H., Hutchison C. A., 3rd Rodent L1 evolution has been driven by a single dominant lineage that has repeatedly acquired new transcriptional regulatory sequences. Mol Biol Evol. 1994 Sep;11(5):778–789. doi: 10.1093/oxfordjournals.molbev.a040158. [DOI] [PubMed] [Google Scholar]
  2. Britten R. J., Baron W. F., Stout D. B., Davidson E. H. Sources and evolution of human Alu repeated sequences. Proc Natl Acad Sci U S A. 1988 Jul;85(13):4770–4774. doi: 10.1073/pnas.85.13.4770. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Burton F. H., Loeb D. D., Voliva C. F., Martin S. L., Edgell M. H., Hutchison C. A., 3rd Conservation throughout mammalia and extensive protein-encoding capacity of the highly repeated DNA long interspersed sequence one. J Mol Biol. 1986 Jan 20;187(2):291–304. doi: 10.1016/0022-2836(86)90235-4. [DOI] [PubMed] [Google Scholar]
  4. Cabot E. L., Angeletti B., Usdin K., Furano A. V. Rapid evolution of a young L1 (LINE-1) clade in recently speciated Rattus taxa. J Mol Evol. 1997 Oct;45(4):412–423. doi: 10.1007/pl00006246. [DOI] [PubMed] [Google Scholar]
  5. Casavant N. C., Hardies S. C. The dynamics of murine LINE-1 subfamily amplification. J Mol Biol. 1994 Aug 19;241(3):390–397. doi: 10.1006/jmbi.1994.1515. [DOI] [PubMed] [Google Scholar]
  6. Casavant N. C., Sherman A. N., Wichman H. A. Two persistent LINE-1 lineages in Peromyscus have unequal rates of evolution. Genetics. 1996 Apr;142(4):1289–1298. doi: 10.1093/genetics/142.4.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Clough J. E., Foster J. A., Barnett M., Wichman H. A. Computer simulation of transposable element evolution: random template and strict master models. J Mol Evol. 1996 Jan;42(1):52–58. doi: 10.1007/BF00163211. [DOI] [PubMed] [Google Scholar]
  8. Deininger P. L., Batzer M. A., Hutchison C. A., 3rd, Edgell M. H. Master genes in mammalian repetitive DNA amplification. Trends Genet. 1992 Sep;8(9):307–311. doi: 10.1016/0168-9525(92)90262-3. [DOI] [PubMed] [Google Scholar]
  9. Edgell M. H., Hardies S. C., Loeb D. D., Shehee W. R., Padgett R. W., Burton F. H., Comer M. B., Casavant N. C., Funk F. D., Hutchison C. A., 3rd The L1 family in mice. Prog Clin Biol Res. 1987;251:107–129. [PubMed] [Google Scholar]
  10. Hattori M., Kuhara S., Takenaka O., Sakaki Y. L1 family of repetitive DNA sequences in primates may be derived from a sequence encoding a reverse transcriptase-related protein. Nature. 1986 Jun 5;321(6070):625–628. doi: 10.1038/321625a0. [DOI] [PubMed] [Google Scholar]
  11. Hohjoh H., Singer M. F. Cytoplasmic ribonucleoprotein complexes containing human LINE-1 protein and RNA. EMBO J. 1996 Feb 1;15(3):630–639. [PMC free article] [PubMed] [Google Scholar]
  12. Holmes S. E., Singer M. F., Swergold G. D. Studies on p40, the leucine zipper motif-containing protein encoded by the first open reading frame of an active human LINE-1 transposable element. J Biol Chem. 1992 Oct 5;267(28):19765–19768. [PubMed] [Google Scholar]
  13. Jurka J., Zietkiewicz E., Labuda D. Ubiquitous mammalian-wide interspersed repeats (MIRs) are molecular fossils from the mesozoic era. Nucleic Acids Res. 1995 Jan 11;23(1):170–175. doi: 10.1093/nar/23.1.170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kolosha V. O., Martin S. L. Polymorphic sequences encoding the first open reading frame protein from LINE-1 ribonucleoprotein particles. J Biol Chem. 1995 Feb 10;270(6):2868–2873. doi: 10.1074/jbc.270.6.2868. [DOI] [PubMed] [Google Scholar]
  15. Loeb D. D., Padgett R. W., Hardies S. C., Shehee W. R., Comer M. B., Edgell M. H., Hutchison C. A., 3rd The sequence of a large L1Md element reveals a tandemly repeated 5' end and several features found in retrotransposons. Mol Cell Biol. 1986 Jan;6(1):168–182. doi: 10.1128/mcb.6.1.168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Martin S. L. LINEs. Curr Opin Genet Dev. 1991 Dec;1(4):505–508. doi: 10.1016/s0959-437x(05)80199-6. [DOI] [PubMed] [Google Scholar]
  17. Modi W. S. Phylogenetic history of LINE-1 among arvicolid rodents. Mol Biol Evol. 1996 May;13(5):633–641. doi: 10.1093/oxfordjournals.molbev.a025623. [DOI] [PubMed] [Google Scholar]
  18. Mülhardt C., Fischer M., Gass P., Simon-Chazottes D., Guénet J. L., Kuhse J., Betz H., Becker C. M. The spastic mouse: aberrant splicing of glycine receptor beta subunit mRNA caused by intronic insertion of L1 element. Neuron. 1994 Oct;13(4):1003–1015. doi: 10.1016/0896-6273(94)90265-8. [DOI] [PubMed] [Google Scholar]
  19. Pascale E., Liu C., Valle E., Usdin K., Furano A. V. The evolution of long interspersed repeated DNA (L1, LINE 1) as revealed by the analysis of an ancient rodent L1 DNA family. J Mol Evol. 1993 Jan;36(1):9–20. doi: 10.1007/BF02407302. [DOI] [PubMed] [Google Scholar]
  20. Rogers J. H. The origin and evolution of retroposons. Int Rev Cytol. 1985;93:187–279. doi: 10.1016/s0074-7696(08)61375-3. [DOI] [PubMed] [Google Scholar]
  21. Shen M. R., Batzer M. A., Deininger P. L. Evolution of the master Alu gene(s). J Mol Evol. 1991 Oct;33(4):311–320. doi: 10.1007/BF02102862. [DOI] [PubMed] [Google Scholar]
  22. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  23. Usdin K., Chevret P., Catzeflis F. M., Verona R., Furano A. V. L1 (LINE-1) retrotransposable elements provide a "fossil" record of the phylogenetic history of murid rodents. Mol Biol Evol. 1995 Jan;12(1):73–82. doi: 10.1093/oxfordjournals.molbev.a040192. [DOI] [PubMed] [Google Scholar]
  24. Verneau O., Catzeflis F., Furano A. V. Determination of the evolutionary relationships in Rattus sensu lato (Rodentia : Muridae) using L1 (LINE-1) amplification events. J Mol Evol. 1997 Oct;45(4):424–436. doi: 10.1007/pl00006247. [DOI] [PubMed] [Google Scholar]
  25. Willard C., Nguyen H. T., Schmid C. W. Existence of at least three distinct Alu subfamilies. J Mol Evol. 1987;26(3):180–186. doi: 10.1007/BF02099850. [DOI] [PubMed] [Google Scholar]
  26. 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]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES