Skip to main content
Log in

Transposable elements and the evolution of genome size in eukaryotes

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

It is generally accepted that the wide variation in genome size observed among eukaryotic species is more closely correlated with the amount of repetitive DNA than with the number of coding genes. Major types of repetitive DNA include transposable elements, satellite DNAs, simple sequences and tandem repeats, but reliable estimates of the relative contributions of these various types to total genome size have been hard to obtain. With the advent of genome sequencing, such information is starting to become available, but no firm conclusions can yet be made from the limited data currently available. Here, the ways in which transposable elements contribute both directly and indirectly to genome size variation are explored. Limited evidence is provided to support the existence of an approximately linear relationship between total transposable element DNA and genome size. Copy numbers per family are low and globally constrained in small genomes, but vary widely in large genomes. Thus, the partial release of transposable element copy number constraints appears to be a major characteristic of large genomes.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Sujatha Thankeswaran Parvathy, Varatharajalu Udayasuriyan & Vijaipal Bhadana

References

  • Adams, M.D., S.E. Celniker, R.A. Holt, C.A. Evans, J.D. Gocayne, P.G. Amanatides, S.E. Scherer, P.W. Li, R.A. Hoskins, R.F. Galle, R.A. George, S.E. Lewis, S. Richards, M. Ashburner, S.N. Henderson, G.G. Sutton, J.R. Wortman, M.D. Yandell, Q. Zhang, L.X. Chen, R.C. Brandon, Y.H. Rogers, R.G. Blazej, M. Champe, B.D. Pfeiffer, K.H. Wan, C. Doyle, E.G. Baxter, G. Helt, C.R. Nelson, G.L. Gabor, J.F. Abril, A. Agbayani, H.J. An, C. Andrews-Pfannkoch, D. Baldwin, R.M. Ballew, A. Basu, J. Baxendale, L. Bayraktaroglu, E.M. Beasley, K.Y. Beeson, P.V. Benos, B.P. Berman, D. Bhandari, S. Bolshakov, D. Borkova, M.R. Botchan, J. Bouck, P. Brokstein, P. Brottier, K.C. Burtis, D.A. Busam, H. Butler, E. Cadieu, A. Center, I. Chandra, J.M. Cherry, S. Cawley, C. Dahlke, L.B. Davenport, P. Davies, B. de Pablos, A. Delcher, Z. Deng, A.D. Mays, I. Dew, S.M. Dietz, K. Dodson, L.E. Doup, M. Downes, S. Dugan-Rocha, B.C. Dunkov, P. Dunn, K.J. Durbin, C.C. Evangelista, C. Ferraz, S. Ferriera, W. Fleischmann, C. Fosler, A.E. Gabrielian, N.S. Garg, W.M. Gelbart, K. Glasser, A. Glodek, F. Gong, J.H. Gorrell, Z. Gu, P. Guan, M. Harris, N.L. Harris, D. Harvey, T.J. Heiman, J.R. Hernandez, J. Houck, D. Hostin, K.A. Houston, T.J. Howland, M.H. Wei, C. Ibegwam, M. Jalali, F. Kalush, G.H. Karpen, Z. Ke, J.A. Kennison, K.A. Ketchum, B.E. Kimmel, C.D. Kodira, C. Kraft, S. Kravitz, D. Kulp, Z. Lai, P. Lasko, Y. Lei, A.A. Levitsky, J. Li, Z. Li, Y. Liang, X. Lin, X. Liu, B. Mattei, T.C. McIntosh, M.P. McLeod, D. McPherson, G. Merkulov, N.V. Milshina, C. Mobarry, J. Morris, A. Moshrefi, S.M. Mount, M. Moy, B. Murphy, L. Murphy, D.M. Muzny, D.L. Nelson, D.R. Nelson, K.A. Nelson, K. Nixon, D.R. Nusskern, J.M. Pacleb, M. Palazzolo, G.S. Pittman, S. Pan, J. Pollard, V. Puri, M.G. Reese, K. Reinert, K. Remington, R.D. Saunders, F. Scheeler, H. Shen, B.C. Shue, I. Siden-Kiamos, M. Simpson, M.P. Skupski, T. Smith, E. Spier, A.C. Spradling, M. Stapleton, R. Strong, E. Sun, R. Svirskas, C. Tector, R. Turner, E. Venter, A.H. Wang, X. Wang, Z.Y. Wang, D.A. Wassarman, G.M. Weinstock, J. Weissenbach, S.M. Williams Woodage, T.K.C. Worley, D. Wu, S. Yang, Q.A. Yao, J. Ye, R.F. Yeh, J.S. Zaveri, M. Zhan, G. Zhang, Q. Zhao, L. Zheng, X.H. Zheng, F.N. Zhong, W. Zhong, X. Zhou, S. Zhu, X. Zhu, H.O. Smith, R.A. Gibbs, E.W. Myers, G.M. Rubin & J.C. Venter. 2000. The genome sequence of Drosophila melanogaster. Science 287: 2185-2195.

    Google Scholar 

  • Ananiev, E.V., R.L. Phillips & H.W. Rines, 1998. Complex structure of knob DNA on maize chromosome 9. Retrotransposon invasion into heterochromatin. Genetics 149: 2025-2037.

    Google Scholar 

  • Bennett, M.D. & J.D. Smith, 1976. Nuclear DNA amounts in angiosperms. Phil. Trans. R. Soc. Lond. B 274: 227-274.

    Google Scholar 

  • Bennetzen, J.L., 2000. Transposable element contributions to plant gene and genome evolution. Plant Mol. Biol. 42: 251-269.

    Google Scholar 

  • Bennetzen, J.L., P. SanMiguel, M. Chen, A. Tikhonov, M. Francki & Z. Avramova, 1998. Grass genomes. Proc. Natl. Acad. Sci. USA 95: 1975-1978.

    Google Scholar 

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

    Google Scholar 

  • Black, W.C.& K.S. Rai, 1988. Genome evolution in mosquitoes: intraspecific and interspecific variation in repetitive DNA amounts and organization. Genet. Res. 51: 185-196.

    Google Scholar 

  • Boeke, J.D. & J.P. Stoye, 1997. Retrotransposons, Endogenous Retroviruses and the Evolution of the Retroelements in Retroviruses, edited by J.M. Coffin, S.H. Hughes & H.E. Varmus. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

    Google Scholar 

  • Bureau, T.E., S.E. White & S.R. Wessler, 1994. Transduction of a cellular gene by a plant retroelement. Cell 77: 479-480.

    Google Scholar 

  • Caceres, M., M. Puig & A. Ruiz, 2001. Molecular characterization of two natural hotspots in the Drosophila buzzatii genome induced by transposon insertions. Genome Res. 11: 1353-1364.

    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.

    Google Scholar 

  • Capy, P., C. Bazin, D. Higuet & T. Langin, 1997. Dynamics and Evolution of Transposable Elements. Landes Bioscience, Austin TX.

    Google Scholar 

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

    Google Scholar 

  • Copenhaver, G.P. & D. Preuss, 1999. Centromeres in the genomic era: unraveling paradoxes. Curr. Opin. Plant Biol. 2: 104-108.

    Google Scholar 

  • Cresse, A.D., S.H. Hulbert, W.E. Brown, J.R. Lucas & J.L. Bennetzen, 1995. Mu1-related transposable elements of maize preferentially insert into low copy number DNA. Genetics 140: 315-324.

    Google Scholar 

  • Deininger, P.L. & M.A. Batzer, 1999. Alu repeats and human disease. Mol. Genet. Metab. 67: 183-193.

    Google Scholar 

  • Dorer, D.R. & S. Henikoff, 1994. Expansions of transgene repeats cause heterochromatin formation and gene silencing in Drosophila. Cell 77: 993-1002.

    Google Scholar 

  • Duret, L., G. Marais & C. Biemont, 2000. Transposons but not retrotransposons are located preferentially in regions of high recombination rate in Caenorhabditis elegans. Genetics 156: 1661-1669.

    Google Scholar 

  • Elgar, G., M.S. Clark, S. Meek, S. Smith, S. Warner, Y.J. Edwards, N. Bouchireb, A. Cottage, G.S. Yeo, Y. Umrania, G. Williams & S. Brenner. 1999. Generation and analysis of 25 Mb of genomic DNA from the pufferfish Fugu rubripes by sequence scanning. Genome Res. 9: 960-971.

    Google Scholar 

  • 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.

    Google Scholar 

  • Fanti, L., D.R. Dorer, M. Berloco, S. Henikoff & S. Pimpinelli, 1998. Heterochromatin protein 1 binds transgene arrays. Chromosoma 107: 286-292.

    Google Scholar 

  • Feschotte, C. & C. Mouches, 2000. Recent amplification of miniature inverted-repeat transposable elements in the vector mosquito Culex pipiens: characterization of the Mimo family. Gene 250: 109-116.

    Google Scholar 

  • Finnegan, D.J., 1989. Eukaryotic transposable elements and genome evolution. Trends Genet. 5: 103-107.

    Google Scholar 

  • Fu, H., W. Park, X. Yan, Z. Zheng, B. Shen & H.K. Dooner, 2001. The highly recombinogenic bz locus lies in an unusually generich region of the maize genome. Proc. Natl. Acad. Sci. USA 98: 8903-8908.

    Google Scholar 

  • Garber, K., I. Bilic, O. Pusch, J. Tohme, A. Bachmair, D. Schweizer & V. Jantsch, 1999. The Tpv2 family of retrotransposons of Phaseolus vulgaris: structure, integration characteristics, and use for genotype classification. Plant Mol. Biol. 39: 797-807.

    Google Scholar 

  • Glockner, G., K. Szafranski, T. Winckler, T. Dingermann, M.A. Quail, E. Cox, L. Eichinger, A.A. Noegel & A. Rosenthal. 2001. The complex repeats of Dictyostelium discoideum. Genome Res. 11: 585-594.

    Google Scholar 

  • Goodier, J.L., E.M. Ostertag & H.H. Kazazian Jr., 2000. Transduction of 361-1flanking sequences is common in L1 retrotransposition. Hum. Mol. Genet. 9: 653-657.

  • Gray, Y.H., 2000. It takes two transposons to tango: transposableelement-mediated chromosomal rearrangements. Trends Genet. 16: 461-468.

    Google Scholar 

  • Green, E.D. & A. Chakravarti, 2001. The human genome sequence expedition: views from the ‘base camp’. Genome Res. 11: 645-651.

    Google Scholar 

  • Gregory, T.R., 2001. Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma. Biol. Rev. Camb. Philos. Soc. 76: 65-101.

    Google Scholar 

  • Gregory, T.R. & P.D. Hebert, 1999. The modulation of DNA content: proximate causes and ultimate consequences. Genome Res. 9: 317-324.

    Google Scholar 

  • Heikkinen, E., V. Launonen, E. Muller & L. Bachmann, 1995. The pvB370 BamIII satellite DNA family of the Drosophila virilis group and its evolutionary relation to mobile dispersed genetic pDv elements. J. Mol. Evol. 41: 604-614.

    Google Scholar 

  • Henikoff, S., E.A. Greene, S. Pietrokovski, P. Bork, T.K. Attwood & L. Hood, 1997. Gene families: the taxonomy of protein paralogs and chimeras. Science 278: 609-614.

    Google Scholar 

  • International Human Genome Sequencing Consortium, 2001. Initial sequencing and analysis of the human genome. Nature 409: 860-921.

    Google Scholar 

  • Jin, Y.K. & J.L. Bennetzen, 1989. Structure and coding properties of Bs1, a maize retrovirus-like transposon. Proc. Natl. Acad. Sci. USA 86: 6235-6239.

    Google Scholar 

  • John, B., 1988. The biology of heterochromatin, pp. 1-128 in Heterochromatin, Molecular and Structural Aspects, edited by R.S. Verma. Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Kalendar, R., J. Tanskanen, S. Immonen, E. Nevo & A.H. Schulman, 2000. Genome evolution of wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. Proc. Natl. Acad. Sci. USA 97: 6603-6607.

    Google Scholar 

  • Kapitonov, V.V., G.P. Holmquist & J. Jurka, 1998. L1 repeat is a basic unit of heterochromatin satellites in Cetaceans. Mol. Biol. Evol. 15: 611-612.

    Google Scholar 

  • Kapitonov, V.V. & J. Jurka, 1999. Molecular paleontology of transposable elements from Arabidopsis thaliana. Genetica 107: 27-37.

    Google Scholar 

  • Kapitonov, V.V. & J. Jurka, 2001. Rolling-circle transposons in eukaryotes. Proc. Natl. Acad. Sci. USA 98: 8714-8719.

    Google Scholar 

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

    Google Scholar 

  • Kidwell, M.G. & D.R. Lisch, 2000. Transposable elements and host genome evolution. Trends Ecol. Evol. 15: 95-99.

    Google Scholar 

  • Kidwell, M.G. & D.R. Lisch, 2001. Perspective: transposable elements, parasitic DNA, and genome evolution. Evolution 55: 1-24.

    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.

    Google Scholar 

  • Kumar, A., 1996. The adventures of the Ty1-copia group of retrotransposons in plants. Trends Genet. 12: 41-43.

    Google Scholar 

  • Kumar, A. & J.L. Bennetzen, 1999. Plant retrotransposons. Annu. Rev. Genet. 33: 479-532.

    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.

    Google Scholar 

  • Le, Q.H., S. Wright, Z. Yu & T. Bureau, 2000. Transposon diversity in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 97: 7376-7381.

    Google Scholar 

  • Levis, R.W., R. Ganesan, K. Houtchens, L.A. Tolar & F.M. Sheen, 1993. Transposons in place of telomeric repeats at a Drosophila telomere. Cell 75: 1083-1093.

    Google Scholar 

  • Lim, J.K. & M.J. Simmons, 1994. Gross chromosome rearrangements mediated by transposable elements in Drosophila melanogaster. Bioessays 16: 269-275.

    Google Scholar 

  • Malik, H.S., S. Henikoff & T.H. Eickbush, 2000. Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses. Genome Res. 10: 1307-1318.

    Google Scholar 

  • McClure, M.A., 1999. The retroid agents: disease, function, and evolution, pp. 163-195 in Origin and Evolution of Viruses, edited by E. Domingo, R. Webster & J. Holland. Academic Press, London.

    Google Scholar 

  • McDonald, J.F., 1998. Transposable elements, gene silencing and macroevolution. Trends Ecol. Evol. 13: 94-95.

    Google Scholar 

  • Miller, W.J., A. Nagel, J. Bachmann & L. Bachmann, 2000. Evolutionary dynamics of the SGM transposon family in the Drosophila obscura species group. Mol. Biol. Evol. 17: 1597-1609.

    Google Scholar 

  • Moran, J.V., R.J. DeBerardinis & H.H. Kazazian Jr., 1999. Exon shuffling by L1 retrotransposition. Science 283: 1530-1534.

    Google Scholar 

  • Nadir, E., H. Margalit, T. Gallily & S.A. Ben-Sasson, 1996. Microsatellite spreading in the human genome: evolutionary mechanisms and structural implications. Proc. Natl. Acad. Sci. USA 93: 6470-6475.

    Google Scholar 

  • Ohno, S., 1970. Gene Duplication. Springer Verlag, Berlin.

    Google Scholar 

  • Okazaki, S., H. Ishikawa & H. Fujiwara, 1995. Structural analysis of TRAS1, a novel family of telomeric repeat-associated retrotransposons in the silkworm, Bombyx mori. Mol. Cell Biol. 15: 4545-4552.

    Google Scholar 

  • Petrov, D.A., 2001. Evolution of genome size: new approaches to an old problem. Trends Genet. 17: 23-28.

    Google Scholar 

  • Pickeral, O.K., W. Makaowski, M.S. Boguski & J.D. Boeke, 2000. Frequent human genomic DNA transduction driven by LINE-1 retrotransposition. Genome Res. 10: 411-415.

    Google Scholar 

  • Pimpinelli, S., M. Berloco, L. Fanti, P. Dimitri, S. Bonaccorsi, E. Marchetti, R. Caizzi, C. Caggese & M. Gatti. 1995. Transposable elements are stable structural components of Drosophila melanogaster heterochromatin. Proc. Natl. Acad. Sci. USA 92: 3804-3808.

    Google Scholar 

  • Rai, K.S. & W.C. Black, 1999. Mosquito genomes: structure, organization and evolution. Adv. Genet. 41: 1-33.

    Google Scholar 

  • Ramsay, L., M. Macaulay, L. Cardle, M. Morgante, S. degli Ivanissevich, E. Maestri, W. Powell & R. Waugh, 1999. Intimate association of microsatellite repeats with retrotransposons and other dispersed repetitive elements in barley. Plant J. 17: 415-425.

    Google Scholar 

  • Roy, A.M., M.L. Carroll, S.V. Nguyen, A.H. Salem, M. Oldridge, A.O. Wilkie, M.A. Batzer & P.L. Deininger, 2000. Potential gene conversion and source genes for recently integrated Alu elements. Genome Res. 10: 1485-1495.

    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.

    Google Scholar 

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

    Google Scholar 

  • Smit, A.F., 1999. Interspersed repeats and other mementos of transposable elements in mammalian genomes. Curr. Opin. Genet. Dev. 9: 657-663.

    Google Scholar 

  • Steinemann, M. & S. Steinemann, 1998. Enigma of Y chromosome degeneration: neo-Y and neo-X chromosomes of Drosophila miranda a model for sex chromosome evolution. Genetica 103: 409-420.

    Google Scholar 

  • The Arabidopsis Genome Initiative, 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.

    Google Scholar 

  • Tikhonov, A.P., P.J. SanMiguel, Y. Nakajima, N.M. Gorenstein, J.L. Bennetzen & Z. Avramova, 1999. Colinearity and its exceptions in orthologous adh regions of maize and sorghum. Proc. Natl. Acad. Sci. USA 96: 7409-7414.

    Google Scholar 

  • Tilford, C.A., T. Kuroda-Kawaguchi, H. Skaletsky, S. Rozen, L.G. Brown, M. Rosenberg, J.D. McPherson, K. Wylie et al., 2001. A physical map of the human Y chromosome. Nature 409: 943-945.

    Google Scholar 

  • Tschiersch, B., A. Hofmann, V. Krauss, R. Dorn, G. Korge & G. Reuter, 1994. The protein encoded by the Drosophila position-effect variegation suppressor gene Su(var)3-9 combines domains of antagonistic regulators of homeotic gene complexes. EMBO J. 13: 3822-3831.

    Google Scholar 

  • Tu, Z., 1997. Three novel families of miniature inverted-repeat transposable elements are associated with genes of the yellow fever mosquito, Aedes aegypti. Proc. Natl. Acad. Sci. USA 94: 7475-7480.

    Google Scholar 

  • Tu, Z., 2000. Molecular and evolutionary analysis of two divergent subfamilies of a novel miniature inverted repeat transposable element in the yellow fever mosquito, Aedes aegypti. Mol. Biol. Evol. 17: 1313-1325.

    Google Scholar 

  • Tu, Z., 2001a. Eight novel families of miniature inverted repeat transposable elements in the African malaria mosquito, Anopheles gambiae. Proc. Natl. Acad. Sci. USA 98: 1699-1704.

    Google Scholar 

  • Tu, Z., 2001b. Maque, a family of extremely short interspersed repetitive elements: characterization, possible mechanism of transposition, and evolutionary implications. Gene 263: 247-253.

    Google Scholar 

  • Turcotte, K., S. Srinivasan & T. Bureau, 2001. Survey of transposable elements from rice genomic sequences. Plant J. 25: 169-179.

    Google Scholar 

  • Vicient, C.M., A. Suoniemi, K. Anamthawat-Jonsson, J. Tanskanen, A. Beharav, E. Nevo & A.H. Schulman, 1999. Retrotransposon BARE-1 and its role in genome evolution in the genus Hordeum. Plant Cell 11: 1769-1784.

    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.

    Google Scholar 

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

    Google Scholar 

  • Wendel, J.F. & S.R. Wessler, 2000. Retrotransposon-mediated genome evolution on a local ecological scale. Proc. Natl. Acad. Sci. USA 97: 6250-6252.

    Google Scholar 

  • Wilder, J. & H. Hollocher, 2001. Mobile elements and the genesis of microsatellites in dipterans. Mol. Biol. Evol. 18: 384-392.

    Google Scholar 

  • Wong, G.K., D.A. Passey, Y. Huang, Z. Yang & J. Yu, 2000. Is ‘junk’ DNA mostly intron DNA? Genome Res. 10: 1672-1678.

    Google Scholar 

  • Yu, Z., S.I. Wright & T.E. Bureau, 2000. Mutator-like elements in Arabidopsis thaliana. Structure, diversity and evolution. Genetics 156: 2019-2031.

    Google Scholar 

  • Zelentsova, E.S., R.P. Vashakidze, A.S. Kraev & M.B. Evgen'ev, 1986. Dispersed repeats in Drosophila virilis: elements mobilized by interspecific hybridization. Chromosoma 93: 469-476.

    Google Scholar 

  • Zhang, Q., J. Arbuckle & S.R. Wessler, 2000. Recent, extensive, and preferential insertion of members of the miniature inverted-repeat transposable element family Heartbreaker into genic regions of maize. Proc. Natl. Acad. Sci. USA 97: 1160-1165.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kidwell, M.G. Transposable elements and the evolution of genome size in eukaryotes. Genetica 115, 49–63 (2002). https://doi.org/10.1023/A:1016072014259

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1016072014259

Navigation