, Volume 115, Issue 1, pp 49–63 | Cite as

Transposable elements and the evolution of genome size in eukaryotes

  • Margaret G. Kidwell


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.

genome size molecular evolution transposable element 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 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
  2. 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
  3. Bennett, M.D. & J.D. Smith, 1976. Nuclear DNA amounts in angiosperms. Phil. Trans. R. Soc. Lond. B 274: 227-274.Google Scholar
  4. Bennetzen, J.L., 2000. Transposable element contributions to plant gene and genome evolution. Plant Mol. Biol. 42: 251-269.Google Scholar
  5. 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
  6. Biémont, C., A. Tsitrone, C. Vieira & C. Hoogland, 1997. Transposable element distribution in Drosophila. Genetics 147: 1997-1999.Google Scholar
  7. 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
  8. 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
  9. 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
  10. 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
  11. 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
  12. Capy, P., C. Bazin, D. Higuet & T. Langin, 1997. Dynamics and Evolution of Transposable Elements. Landes Bioscience, Austin TX.Google Scholar
  13. Charlesworth, B., C.H. Langley & P.D. Sniegowski, 1997. Transposable element distributions in Drosophila. Genetics 147: 1993-1995.Google Scholar
  14. Copenhaver, G.P. & D. Preuss, 1999. Centromeres in the genomic era: unraveling paradoxes. Curr. Opin. Plant Biol. 2: 104-108.Google Scholar
  15. 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
  16. Deininger, P.L. & M.A. Batzer, 1999. Alu repeats and human disease. Mol. Genet. Metab. 67: 183-193.Google Scholar
  17. Dorer, D.R. & S. Henikoff, 1994. Expansions of transgene repeats cause heterochromatin formation and gene silencing in Drosophila. Cell 77: 993-1002.Google Scholar
  18. 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
  19. 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
  20. 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
  21. Fanti, L., D.R. Dorer, M. Berloco, S. Henikoff & S. Pimpinelli, 1998. Heterochromatin protein 1 binds transgene arrays. Chromosoma 107: 286-292.Google Scholar
  22. 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
  23. Finnegan, D.J., 1989. Eukaryotic transposable elements and genome evolution. Trends Genet. 5: 103-107.Google Scholar
  24. 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
  25. 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
  26. 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
  27. 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.Google Scholar
  28. Gray, Y.H., 2000. It takes two transposons to tango: transposableelement-mediated chromosomal rearrangements. Trends Genet. 16: 461-468.Google Scholar
  29. Green, E.D. & A. Chakravarti, 2001. The human genome sequence expedition: views from the ‘base camp’. Genome Res. 11: 645-651.Google Scholar
  30. 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
  31. Gregory, T.R. & P.D. Hebert, 1999. The modulation of DNA content: proximate causes and ultimate consequences. Genome Res. 9: 317-324.Google Scholar
  32. 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
  33. 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
  34. International Human Genome Sequencing Consortium, 2001. Initial sequencing and analysis of the human genome. Nature 409: 860-921.Google Scholar
  35. 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
  36. 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
  37. 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
  38. 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
  39. Kapitonov, V.V. & J. Jurka, 1999. Molecular paleontology of transposable elements from Arabidopsis thaliana. Genetica 107: 27-37.Google Scholar
  40. Kapitonov, V.V. & J. Jurka, 2001. Rolling-circle transposons in eukaryotes. Proc. Natl. Acad. Sci. USA 98: 8714-8719.Google Scholar
  41. Kidwell, M.G., 1993. Lateral transfer in natural populations of eukaryotes. Ann. Rev. Genet. 27: 235-256.Google Scholar
  42. Kidwell, M.G. & D.R. Lisch, 2000. Transposable elements and host genome evolution. Trends Ecol. Evol. 15: 95-99.Google Scholar
  43. Kidwell, M.G. & D.R. Lisch, 2001. Perspective: transposable elements, parasitic DNA, and genome evolution. Evolution 55: 1-24.Google Scholar
  44. 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
  45. Kumar, A., 1996. The adventures of the Ty1-copia group of retrotransposons in plants. Trends Genet. 12: 41-43.Google Scholar
  46. Kumar, A. & J.L. Bennetzen, 1999. Plant retrotransposons. Annu. Rev. Genet. 33: 479-532.Google Scholar
  47. 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
  48. 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
  49. 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
  50. Lim, J.K. & M.J. Simmons, 1994. Gross chromosome rearrangements mediated by transposable elements in Drosophila melanogaster. Bioessays 16: 269-275.Google Scholar
  51. 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
  52. 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
  53. McDonald, J.F., 1998. Transposable elements, gene silencing and macroevolution. Trends Ecol. Evol. 13: 94-95.Google Scholar
  54. 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
  55. Moran, J.V., R.J. DeBerardinis & H.H. Kazazian Jr., 1999. Exon shuffling by L1 retrotransposition. Science 283: 1530-1534.Google Scholar
  56. 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
  57. Ohno, S., 1970. Gene Duplication. Springer Verlag, Berlin.Google Scholar
  58. 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
  59. Petrov, D.A., 2001. Evolution of genome size: new approaches to an old problem. Trends Genet. 17: 23-28.Google Scholar
  60. 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
  61. 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
  62. Rai, K.S. & W.C. Black, 1999. Mosquito genomes: structure, organization and evolution. Adv. Genet. 41: 1-33.Google Scholar
  63. 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
  64. 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
  65. 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
  66. 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
  67. Smit, A.F., 1999. Interspersed repeats and other mementos of transposable elements in mammalian genomes. Curr. Opin. Genet. Dev. 9: 657-663.Google Scholar
  68. 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
  69. The Arabidopsis Genome Initiative, 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796-815.Google Scholar
  70. 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
  71. 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
  72. 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
  73. 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
  74. 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
  75. 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
  76. 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
  77. Turcotte, K., S. Srinivasan & T. Bureau, 2001. Survey of transposable elements from rice genomic sequences. Plant J. 25: 169-179.Google Scholar
  78. 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
  79. 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
  80. Waterston, R. & J. Sulston, 1995. The genome of Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 92: 10836-10840.Google Scholar
  81. 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
  82. Wilder, J. & H. Hollocher, 2001. Mobile elements and the genesis of microsatellites in dipterans. Mol. Biol. Evol. 18: 384-392.Google Scholar
  83. 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
  84. 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
  85. 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
  86. 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

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Margaret G. Kidwell
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyThe University of ArizonaTucsonUSA (Phone

Personalised recommendations