Skip to main content
SpringerLink
Log in

How valuable are model organisms for transposable element studies?

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Model organisms have proved to be highly informative for many types of genetic studies involving ‘conventional’ genes. The results have often been successfully generalized to other closely related organisms and also, perhaps surprisingly frequently, to more distantly related organisms. Because of the wealth of previous knowledge and their availability and convenience, model organisms were often the species of choice for many of the earlier studies of transposable elements. The question arises whether the results of genetic studies of transposable elements in model organisms can be extrapolated in the same ways as those of conventional genes? A number of observations suggest that special care needs to be taken in generalizing the results from model organisms to other species. A hallmark of many transposable elements is their ability to amplify rapidly in species genomes. Rapid spread of a newly invaded element throughout a species range has also been demonstrated. The types and genomic copy numbers of transposable elements have been shown to differ greatly between some closely related species. Horizontal transfer of transposable elements appears to be more frequent than for nonmobile genes. Furthermore, the population structure of some model organisms has been subject to drastic recent changes that may have some bearing on their transposable element genomic complements. In order to initiate discussion of this question, several case studies of transposable elements in well-studied Drosophila species are presented.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anxolabéhère, D., M.G. Kidwell & G. Périquet, 1988. Molecular characteristics of diverse populations are consistent with the hypothesis of a recent invasion of Drosophila melanogaster by mobile P elements. Mol. Biol. Evol. 5: 252–269.

    PubMed  Google Scholar 

  • Barakat, A., G. Matassi & G. Bernardi, 1998. Distribution of genes in the genome of Arabidopsis thaliana and its implications for the genome organization of plants. Proc. Natl. Acad. Sci. USA 95: 10044–10049.

    Article  PubMed  CAS  Google Scholar 

  • Biemont, C. & G. Cizeron, 1999. Distribution of transposable elements in Drosophila species. Genetica 105: 43–62.

    Article  PubMed  CAS  Google Scholar 

  • Biemont, C., S. Ronsseray, D. Anxolabéhère, H. Izaabel & C. Gautier, 1990. Localization of P elements, copy number regulation, and cytotype determination in Drosophila melanogaster. Genet. Res. 56: 3–14.

    PubMed  CAS  Google Scholar 

  • Biemont, C., A. Tsitrone, C. Vieira & C. Hoogland, 1997. Transposable element distribution in Drosophila. Genetics 147: 1997–1999.

    PubMed  CAS  Google Scholar 

  • Blackman, R., R. Grimaila, M. Koehler & W. Gelbart, 1987. Mobilization of hobo elements residing within the decapentaplegic gene complex: suggestion of a new hybrid dysgenesis system in Drosophila melanogaster. Cell. 49: 497–505.

    Article  PubMed  CAS  Google Scholar 

  • Bucheton, A., R. Paro, H.M. Sang, A. Pelisson & D.J. Finnegan, 1984. The molecular basis of I-R hybrid dysgenesis: identification, cloning and properties of the I factor. Cell. 38: 153–163.

    Article  PubMed  CAS  Google Scholar 

  • Bucheton, A., C. Vaury, M.C. Chaboissier, P. Abad, A. Pelisson & M. Simonelig, 1992. I elements and the Drosophila genome. Genetica 86: 175–190.

    Article  PubMed  CAS  Google Scholar 

  • Caceres, M., J.M. Ranz, A. Barbadilla, M. Long & A. Ruiz, 1999. Generation of a widespread Drosophila inversion by a transposable element. Science 285: 415–418.

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth, B., C.H. Langley & P.D. Sniegowski, 1997. Transposable element distributions in Drosophila. Genetics 147: 1993–1995.

    PubMed  CAS  Google Scholar 

  • Clark, J.B., T.K. Altheide, M.J. Schlosser & M.G. Kidwell, 1995. Molecular evolution of P transposable elements in the genus Drosophila. I. The saltans and willistoni species groups. Mol. Biol. Evol. 12: 902–913.

    PubMed  CAS  Google Scholar 

  • Clark, J.B. & M.G. Kidwell, 1997. A phylogenetic perspective on P transposable element evolution in Drosophila. Proc. Natl. Acad. Sci. USA 94: 11428–11433.

    Article  PubMed  CAS  Google Scholar 

  • Daniels, S.B., K.R. Peterson, L.D. Strausbaugh, M.G. Kidwell & A. Chovnick, 1990. Evidence for horizontal transmission of the P transposable element between Drosophila species. Genetics 124: 339–355.

    PubMed  CAS  Google Scholar 

  • Dowsett, A.P. & M.W. Young, 1982. Differing levels of dispersed repetitive DNA among closely related species of Drosophila. Proc. Natl. Acad. Sci. USA 79: 4570–4574.

    Article  PubMed  CAS  Google Scholar 

  • Ehrman, L. & J.R. Powell, 1982. The Drosophila willistoni species group, pp. 193–225, in The Genetics and Biology of Drosophila, Vol. 3b, edited by M. Ashburner, H.L. Carson and J.N. Thompson, Academic Press, London.

    Google Scholar 

  • Engels, W.R., 1992. The origin of P elements in Drosophila melanogaster. Bioessays 14: 681–686.

    Article  PubMed  CAS  Google Scholar 

  • Evgen'ev, M., H. Zelentsova, L. Mnjoian, H. Poluectova & M.G. Kidwell, 2000. Invasion of Drosophila virilis by the Penelope transposable element. Chromosoma (In Press).

  • Evgen'ev, M.B., G.N. Yenikolopov, N.I. Peunova & Y.V. Ilyin, 1982. Transposition of mobile genetic elements in interspecific hybrids of Drosophila. Chromosoma 85: 375–386.

    Article  PubMed  Google Scholar 

  • Evgen'ev, M.B., H. Zelentsova, N. Shostak, M. Kozitsina, V. Barsky, D.-H. Lankenau & V.G. Corces, 1997. Penelope, a new family of transposable elements and its possible role in hybrid dysgenesis in Drosophila virilis. Proc. Natl. Acad. Sci. USA 94: 196–201.

    Article  PubMed  Google Scholar 

  • Fujii, S., 1942. Further studies on the salivary gland chromosomes of Drosophila virilis. Cytologia 12: 435–459.

    Google Scholar 

  • Gloor, G.B., C.R. Preston, D.M. Johnson-Schlitz, N.A. Nassif, R.W. Phillis, W.K. Benz, H.M. Robertson & W.R. Engels, 1993. Type I repressors of P element mobility. Genetics 135: 81–95.

    PubMed  CAS  Google Scholar 

  • Gubenko, I.S. & M.B. Evgen'ev, 1984. Cytological and linkage maps of Drosophila virilis chromosomes. Genetica 65: 127–139.

    Article  Google Scholar 

  • Hagemann, S., E. Haring & W. Pinsker, 1996. Repeated horizontal transfer of P transposons between Scaptomyza pallida and Drosophila bifasciata. Genetica 98: 43–51.

    Article  PubMed  CAS  Google Scholar 

  • Hsu, T.C., 1952. Chromosomal variation and evolution in the virilis group of Drosophila. Univ. Texas Pub. 5204: 35–72.

    Google Scholar 

  • Hyytia, P., P. Capy, J.R. David & R.S. Singh, 1985. Enzymatic and quantitative variation in European and African populations of Drosophila simulans. Heredity (Edinburgh) 54: 209–217.

    Google Scholar 

  • Jordan, I.K., L.V. Matyunina & J.F. McDonald, 1999. Evidence for the recent horizontal transfer of long terminal repeat retrotransposon. Proc. Natl. Acad. Sci. USA 96: 12621–12625.

    Article  PubMed  CAS  Google Scholar 

  • Kazazian, H.H., Jr. & J.V. Moran, 1998. The impact of L1 retro-transposons on the human genome. Nat. Genet. 19: 19–24.

    PubMed  CAS  Google Scholar 

  • Kidwell, M.G., 1983. Evolution of hybrid dysgenesis determinants in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 80: 1655–1659.

    Article  PubMed  CAS  Google Scholar 

  • Kidwell, M.G., 1993. Lateral transfer in natural populations of eukaryotes. Ann. Rev. Genet. 27: 235–256.

    Article  PubMed  CAS  Google Scholar 

  • Kidwell, M.G., 1994a. The evolutionary history of the P family of transposable elements. J. Heredity 85: 339–346.

    CAS  Google Scholar 

  • Kidwell, M.G., 1994b. The Wilhelmine E. Key 1991 Invitational Lecture. The evolutionary history of the P family of transposable elements. J. Hered 85: 339–346.

    PubMed  CAS  Google Scholar 

  • Kidwell, M.G., J.F. Kidwell & J.A. Sved, 1977. Hybrid dysgenesis in Drosophila melanogaster: A syndrome of aberrant traits including mutation, sterility & male recombination. Genetics 36: 813–833.

    Google Scholar 

  • Kim, J.M., S. Vanguri, J.D. Boeke, A. Gabriel & D.F. Voytas, 1998. Transposable elements and genome organization: A comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res. 8: 464–478.

    PubMed  CAS  Google Scholar 

  • Kimura, K. & M.G. Kidwell, 1994. Differences in P element population dynamics between the sibling species Drosophila melanogaster and Drosophila simulans. Genet. Res. 63: 27–38.

    PubMed  CAS  Google Scholar 

  • Kordis, D. & F. Gubensek, 1998. Unusual horizontal transfer of a long interspersed nuclear element between distant vertebrate classes. Proc. Natl. Acad. Sci. USA 95: 10704–10709.

    Article  PubMed  CAS  Google Scholar 

  • Koshland, D.E., 1988. Biological systems. Science 240: 1385.

    PubMed  Google Scholar 

  • Langley, C.H., E. Montgomery, R. Hudson, N. Kaplan & B. Charlesworth, 1988. On the role of unequal exchange on the containment of transposable element copy number. Genet. Res. 52: 223–235.

    Article  PubMed  CAS  Google Scholar 

  • Lozovskaya, E.R., V.S. Scheinker & M.B. Evgen'ev, 1990. A hybrid dysgenesis syndrome in Drosophila virilis. Genetics 126: 619–623.

    PubMed  CAS  Google Scholar 

  • O'Hare, K. & G.M. Rubin, 1983. Structures of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome. Cell. 34: 25–35.

    Article  PubMed  Google Scholar 

  • Patterson, J.T., 1941. The virilis group of Drosophila in Texas. Amer. Nat. 75: 523–529.

    Article  Google Scholar 

  • Petrov, D.A., J.L. Schutzman, D.L. Hartl & E.R. Lozovskaya, 1995. Diverse transposable elements are mobilized in hybrid dysgenesis in Drosophila virilis. Proc. Natl. Acad. Sci. 92: 8050–8054.

    Article  PubMed  CAS  Google Scholar 

  • Regner, L.P., M.S. Pereira, C.E. Alonso, E. Abdelhay & V.L. Valente, 1996. Genomic distribution of P elements in Drosophila willistoni and a search for their relationship with chromosomal inversions. J. Hered 87: 191–198.

    PubMed  CAS  Google Scholar 

  • Robertson, H.M., 1997. Multiple mariner transposons in flatworms and hydras are related to those of insects. J. Hered. 88: 195–201.

    PubMed  CAS  Google Scholar 

  • Roy, A.M., M.L. Carroll, D.H. Kass, S.V. Nguyen, A.-H. Salem, M.A. Batzer & P.L. Deininger, 1999. Recently integrated human Alu repeats: finding needles in the haystack. Genetica 107: 149–161.

    Article  PubMed  CAS  Google Scholar 

  • SanMiguel, P., B.S. Gaut, A. Tikhonov, Y. Nakajima & J.L. Bennetzen, 1998. The paleontology of intergene retrotransposons of maize. Nat. Genet. 20: 43–45.

    Article  PubMed  CAS  Google Scholar 

  • SanMiguel, P., A. Tikhonov, Y.K. Jin, N. Motchoulskaia, D. Zakharov, A. Melake-Berhan, P.S. Springer & K.J. Edwards, 1996. Nested retrotransposons in the intergenic regions of the maize genome. Science 274: 765–768.

    Article  PubMed  CAS  Google Scholar 

  • Scheinker, S.V., E.R. Lozovskaya, J.G. Bishop, V.G. Corces & M.B. Evgen'ev, 1990. A long terminal repeat-containing retrotransposon is mobilized during hybrid dysgenesis in Drosophila virilis. Proc. Natl. Acad. Sci. USA 87: 9615–9619.

    Article  PubMed  CAS  Google Scholar 

  • Simmons, G.M., 1992. Horizontal transfer of hobo transposable elements with in the Drosophila melanogaster species complex: evidence from DNA sequencing. Mol. Biol. Evol. 9: 1050–1060.

    PubMed  CAS  Google Scholar 

  • Singh, R.S., M. Choudhary & J.R. David, 1987. Contrasting patterns of geographic variation in the cosmopolitan sibling species Drosophila melanogaster and Drosophila simulans. Biochem. Genet. 25: 27–40.

    Article  PubMed  CAS  Google Scholar 

  • Vieira, C., D. Lepetit, S. Dumont & C. Biemont, 1999. Wake up of transposable elements following Drosophila simulans worldwide colonization. Mol. Biol. Evol. 16: 1251–1255.

    PubMed  CAS  Google Scholar 

  • Vieira, J., C.P. Vieira, D.L. Hartl & E.R. Lozovskaya, 1998. Factors contributing to the hybrid dysgenesis syndrome in Drosophila virilis. Genet. Res. 71: 109–117.

    Article  PubMed  CAS  Google Scholar 

  • Warters, M., 1944. Chromosomal aberrations in wild populations of Drosophila. Univ. Texas Pub. 4445: 129–174.

    Google Scholar 

  • Wasserman, M. & F. Wasserman, 1992. Polymorphism in island species of Drosophila. Evol. Biol. 26: 351–381.

    Google Scholar 

  • Waterston, R. & J. Sulston, 1995. The genome of Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 92: 10836–10840.

    Article  PubMed  CAS  Google Scholar 

  • Wright, D.A., N. Ke, J. Smalle, B.M. Hauge, H.M. Goodman & D.F. Voytas, 1996. Multiple non-LTR retrotransposons in the genome of Arabidopsis thaliana. Genetics 142: 569–578.

    PubMed  CAS  Google Scholar 

  • Zelentsova, H., H. Poluectova, L. Mnjoian, G. Lyozin, V. Veleikod-vorskaja, L. Zhivotovsky, M.G. Kidwell & M.B. Evgen'ev, 1999. Distribution and evolution of mobile elements in the virilis species group of Drosophila. Chromosoma 108: 443–456.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, The University of Arizona, 116 BSW Building, Tucson, AZ, 85721, USA (Phone: (

    Margaret G. Kidwell

  2. Engelhardt Institute of Molecular Biology, Vavilov, 32, Moscow, Russia

    Michael B. Evgen'ev

Authors
  1. Margaret G. Kidwell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael B. Evgen'ev
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kidwell, M.G., Evgen'ev, M.B. How valuable are model organisms for transposable element studies?. Genetica 107, 103–111 (1999). https://doi.org/10.1023/A:1003933419159

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1003933419159

Search

Navigation