Advertisement

Chromosome Research

, 19:777 | Cite as

Co-evolution between transposable elements and their hosts: a major factor in genome size evolution?

  • J. Arvid Ågren
  • Stephen I. WrightEmail author
Article

Abstract

Most models of genome size evolution emphasize changes in relative rates of and/or the efficacy of selection on insertions and deletions. However, transposable elements (TEs) are a major contributor to genome size evolution, and since they experience their own selective pressures for expansion, genome size changes may in part be driven by the dynamics of co-evolution between TEs and their hosts. Under this perspective, predictions about the conditions that allow for genome expansion may be altered. In this review, we outline the evidence for TE–host co-evolution, discuss the conditions under which these dynamics can change, and explore the possible contribution to the evolution of genome size. Aided partly by advances in our understanding of the mechanisms of TE silencing via small RNAs, there is growing evidence that the evolution of transposition rates can be important in driving genome expansion and contraction. Shifts in genome size and transposon abundance associated with interspecific hybridization and changes in mating system are consistent with an important role for transposition rate evolution, although other possible explanations persist. More understanding of the potential for the breakdown of host silencing mechanisms and/or the potential for TEs to evade host immune responses will improve our understanding of the importance of changes in TE activity in driving genome size evolution.

Keywords

transposable elements genome size co-evolution molecular evolution 

Abbreviations

LTR

Long terminal repeat

MITE

Miniature inverted repeat transposable element

piRNA

piwi-interacting RNA

siRNA

small interfering RNA

TE

Transposable element

References

  1. Albach DC, Greilhuber J (2004) Genome size variation and evolution in Veronica. Ann Bot 94:897–911PubMedCrossRefGoogle Scholar
  2. Almeida R, Allshire RC (2005) RNA silencing and genome regulation. Trends Cell Biol 15:251–258PubMedCrossRefGoogle Scholar
  3. Aravin AA, Hannon GJ, Brennecke J (2007) The piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318:761–764PubMedCrossRefGoogle Scholar
  4. Baack EJ, Whitney KD, Rieseberg LH (2005) Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species. New Phytol 167:623–630PubMedCrossRefGoogle Scholar
  5. Bennet MD, Leitch IJ (2005) Genome size evolution in plants. In: Gregory TR (ed) The evolution of the genome. Elsevier, AmsterdamGoogle Scholar
  6. Blumenstiel JP (2011) Evolutionary dynamics of transposable elements in a small RNA world. Trends Genet 27:23–31PubMedCrossRefGoogle Scholar
  7. Blumenstiel JP, Hartl DL (2005) Evidence for maternally transmitted small interfering RNA in the repression of transposition in Drosophila virilis. Proc Natl Acad Sci USA 102:15965–15970PubMedCrossRefGoogle Scholar
  8. Brennecke J, Aravin AA, Stark A et al (2007) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128(6):1089–1103PubMedCrossRefGoogle Scholar
  9. Charlesworth B, Barton N (2004) Genome size: does bigger mean worse? Curr Biol 14:R233–R235PubMedCrossRefGoogle Scholar
  10. Charlesworth B, Langley CH (1986) The evolution of self-regulated transposition of transposable elements. Genetics 112:359–383PubMedGoogle Scholar
  11. Charlesworth B, Langley CH (1989) The population genetics of Drosophila transposable elements. Annu Rev Genet 22:251–287CrossRefGoogle Scholar
  12. Cui H, Fedoroff NV (2002) Inducible DNA demethylation mediated by the maize Suppressor-mutator transposon-encoded TnpA protein. Plant Cell 14:2883–2899PubMedCrossRefGoogle Scholar
  13. Desset S, Meignin C, Dastugue B, Vaury C (2003) COM, a heterochromatic locus governing the control of independent endogenous retrovirus from Drosophila melanogaster. Genetics 164:501–509PubMedGoogle Scholar
  14. Dolgin ES, Charlesworth B (2006) The fate of transposable elements in asexual populations. Genetics 174:817–827PubMedCrossRefGoogle Scholar
  15. Gilbert C, Schaack S, Pace JK II, Brindley PJ, Feschotte C (2010) A role for host–parasite interactions in the horizontal transfer of transposons across phyla. Nature 464:1347–1350PubMedCrossRefGoogle Scholar
  16. González J, Petrov D (2009) Genetics. MITEs—the ultimate parasites. Science 325:1352–1353PubMedCrossRefGoogle Scholar
  17. Govindaraju DR, Cullis CA (1991) Modulation of genome size in plants—the influence of breeding systems and neighborhood size. Evol Trends Plants 5:43–51Google Scholar
  18. Gregory TR (2004) Insertion–deletion biases and the evolution of genome size. Gene 324:15–34PubMedCrossRefGoogle Scholar
  19. Gregory TR (2005) The evolution of the genome. Elsevier, Amsterdam, pp 89–162Google Scholar
  20. Grivna ST, Beyret E, Wang Z, Lin H (2006) A novel class of small RNAs in mouse spermatogenic cells. Genes Dev 20:1709–1714PubMedCrossRefGoogle Scholar
  21. Hanada K, Vallejo V, Nobuta K et al (2009) The functional role of pack-MULEs in rice inferred from purifying selection and expression profile. Plant Cell 21:25–38PubMedCrossRefGoogle Scholar
  22. Hawkins JS, Kim H, Nason JD, Wing RA, Wendel JF (2006) Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. Genome Res 16:1252–1261PubMedCrossRefGoogle Scholar
  23. Hollister JD, Gaut BS (2009) Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res 19:1419–1428PubMedCrossRefGoogle Scholar
  24. Hollister JD, Smith LM, Guo Y, Ott F, Weigel D, Gaut BS (2011) Transposable elements and small RNAs contribute to gene expression divergence between Arabidopsis thaliana and Arabidopsis lyrata. Proc Natl Acad Sci USA 108:2322–2327PubMedCrossRefGoogle Scholar
  25. Hu TT, Pattyn P, Bakker EG et al (2011) The Arabidopsis lyrata genome sequence and the basis of rapid genome size change in Arabidopsis. Nat Genet 43:476–481PubMedCrossRefGoogle Scholar
  26. Hutvágner G, Zamore PD (2002) A microRNA in a multiple-turnover RNAi enzyme complex. Science 297:2056–2060PubMedCrossRefGoogle Scholar
  27. International Brachypodium Initiative (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463:763–768CrossRefGoogle Scholar
  28. International Human Genome Sequencing Consortium (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921CrossRefGoogle Scholar
  29. Jian N, Bao Z, Zhang X, Eddy SR, Wessler SR (2004) Pack-MULE transposable elements mediate gene evolution in plants. Nature 431:569–573CrossRefGoogle Scholar
  30. Josefsson C, Dilkes B, Comai L (2006) Parent-dependent loss of gene silencing during interspecies hybridization. Curr Biol 16:322–1328CrossRefGoogle Scholar
  31. Juretic N, Hoen DR, Huynh ML, Harrison PM, Bureau TE (2005) The evolutionary fate of MULE-mediated duplications of host gene fragments in rice. Genome Res 15:1292–1297PubMedCrossRefGoogle Scholar
  32. Kawakami T, Strakosh SC, Zhen Y, Ungerer MC (2010) Different scales of Ty1/copia-like retrotransposon proliferation in the genomes of three diploid hybrid sunflower species. Heredity 104:341–350PubMedCrossRefGoogle Scholar
  33. King KC, Delph LF, Jokela J, Lively CM (2009) The geographic mosaic of sex and the red queen. Curr Biol 19:1438–1441PubMedCrossRefGoogle Scholar
  34. Kolaczkowski B, Hupalo DN, Kern AD (2010) Recurrent adaptation in RNA-interference genes across the Drosophila phylogeny. Mol Biol Evol 24:1–12Google Scholar
  35. Lai Z, Nakazato T, Salmaso M et al (2005a) Extensive chromosomal repatterning and the evolution of sterility barriers in hybrid sunflower species. Genetics 171:291–303PubMedCrossRefGoogle Scholar
  36. Lai J, Li Y, Messing J, Dooner HK (2005b) Gene movement by helitron transposons contributes to the haplotype variability of maize. Proc Natl Acad Sci 102:9068–9073PubMedCrossRefGoogle Scholar
  37. Lisch D (2005) Pack-MULEs: theft on a massive scale. BioEssays 27:353–355PubMedCrossRefGoogle Scholar
  38. Lisch D (2009) Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol 60:43–66PubMedCrossRefGoogle Scholar
  39. Lister R, O'Malley RC, Tonti-Fillippini J et al (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133:523–536PubMedCrossRefGoogle Scholar
  40. Lockton S, Gaut BS (2010) The evolution of transposable elements in natural population of self-fertilizing Arabidopsis thaliana and its outcrossing relative Arabidopsis lyrata. BMC Evol Biol 10:10PubMedCrossRefGoogle Scholar
  41. Lockton S, Ross-Ibarra J, Gaut BS (2008) Demography and weak selection drives patterns of transposable element diversity in natural populations of Arabidopsis lyrata. Proc Natl Acad Sci USA 105:13965–13970PubMedCrossRefGoogle Scholar
  42. Lozovskaya ER, Scheinker VS, Evgen'ev MB (1990) A hybrid dysgenesis syndrome in Drosophila virilis. Genetics 126:619–623PubMedGoogle Scholar
  43. Lu J, Clark AG (2010) Population dynamics of PIWI-interacting RNAs (piRNAs) and their targets in Drosophila. Genome Res 20:212–227PubMedCrossRefGoogle Scholar
  44. Lynch M (2007) The origins of genome architecture. Sinauer Associates, SunderlandGoogle Scholar
  45. Lynch M (2011) Statistical inference on the mechanisms of genome evolution. PLoS Genet 7:e1001389. doi: 10.1371/journal.pgen.1001389 PubMedCrossRefGoogle Scholar
  46. Lynch M, Conery JS (2003) The origins of genome complexity. Science 302:1401–1404PubMedCrossRefGoogle Scholar
  47. Lyozin GT, Makarova KS, Veikodvorskaja VV et al (2001) The structure and evolution of Penelope in the virilis species group of Drosophila: an ancient lineage of retroelements. J Mol Evol 52:445–456PubMedGoogle Scholar
  48. Madlung A, Tyagi AP, Watson B et al (2005) Genomic changes in synthetic Arabidopsis polyploids. Plant J 41:221–230PubMedCrossRefGoogle Scholar
  49. Malone CD, Hannon GJ (2009) Small RNAs as guardians of the genome. Cell 136:656–668PubMedCrossRefGoogle Scholar
  50. Matzke M, Kanno T, Daxinger L, Huettel B, Matzke AJ (2009) RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 21:367–376PubMedCrossRefGoogle Scholar
  51. Morgan M (2001) Transposable element number in mixed mating populations. Genet Res 77:261–275PubMedCrossRefGoogle Scholar
  52. Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A (2005) Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet 37:997–1002PubMedCrossRefGoogle Scholar
  53. Muotri AR, Marchetto MCN, Coufai NG, Gage FH (2007) The necessary junk: new functions for transposable elements. Hum Mol Genet 16:159–167CrossRefGoogle Scholar
  54. Nuzhdin SV, Pasyukova EG, Morozova EA, Flavell AJ (1998) Quantitative genetic analysis of copia retrotransposon activity in inbred Drosophila melanogaster lines. Genetics 150:755–766PubMedGoogle Scholar
  55. Obbard DJ, Gordon KHJ, Buck AH, Jiggins FM (2009) The evolution of RNAi as a defence against viruses and transposable elements. Phil Trans R Soc B 364:99–115PubMedCrossRefGoogle Scholar
  56. Obbard DJ, Jiggins FM, Bradshaw NJ, Little TJ (2010) Recent and recurrent selective sweeps of the antiviral RNAi gene Argonaute-2 in three species of Drosophila. Mol Biol Evol 28:1043–1056PubMedCrossRefGoogle Scholar
  57. Orgel LE, Crick FH (1980) Selfish DNA: the ultimate parasite. Nature 284:604–607PubMedCrossRefGoogle Scholar
  58. Pagel M, Johnstone RA (1992) Variation across species in the size of the nuclear genome supports the junk-DNA explanation for the C-value paradox. Proc R Soc Lond B 249:119–124CrossRefGoogle Scholar
  59. Pannell JR (2009) Mating-system evolution: succeeding by celibacy. Curr Biol 19:983–985CrossRefGoogle Scholar
  60. Paterson AH, Bowers JE, Bruggmann R et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556PubMedCrossRefGoogle Scholar
  61. Petrov DA (2001) Evolution of genome size: new approaches to an old problem. Trends Genet 17:23–28PubMedCrossRefGoogle Scholar
  62. Petrov DA, Schutzman JL, Hartl DL, Lozovksaya ER (1995) Diverse transposable elements are mobilized in hybrid dysgenesis in Drosophila virilis. Proc Natl Acad Sci USA 92:8050–8054PubMedCrossRefGoogle Scholar
  63. Petrov DA, Sangster TA, Johnston JS, Hartl DL, Shaw KL (2000) Evidence for DNA loss as a determinant of genome size. Science 287:1060–1062PubMedCrossRefGoogle Scholar
  64. Pettersson ME, Kurland CG, Berg OG (2009) Deletion rate evolution and its effect on genome size and coding density. Mol Biol Evol 26:1421–1430PubMedCrossRefGoogle Scholar
  65. Piegu B, Guoyot R, Picault N et al (2006) Doubling genome size without polyploidization: dynamics of retrotransposon-mediated genome expansion in Oryza australiensis, a wild relative of rice. Genome Res 16:1262–1269PubMedCrossRefGoogle Scholar
  66. Prud'homme NM, Masson GM, Terzian C, Bucheteon A (1995) Flamenco a gene controlling the gypsy retrovirus of Drosophila melanogaster. Genetics 139:697–711PubMedGoogle Scholar
  67. Rieseberg LH (1997) Hybrid origins of plant species. Annu Rev Ecol Syst 28:359–389CrossRefGoogle Scholar
  68. Rieseberg LH, Beckstrom-Sternberg SM, Liston, Arias DM (1991) Phylogenetic and systematic inferences from chloroplast DNA and isozyme variation in Helianthus sect. Helianthus (Asteraceae). Syst Bot 16:50–76CrossRefGoogle Scholar
  69. Roth BM, Pruss GJ, Vance VB (2004) Plant viral suppressors of RNA silencing. Virus Res 102:97–108PubMedCrossRefGoogle Scholar
  70. Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115PubMedCrossRefGoogle Scholar
  71. Shan XH, Liu ZL, Dong ZY et al (2005) Mobilization of the active MITE transposons mPing and Pong in rice by introgression from wild rice (Zizania latifolia Griseb.). Mol Biol Evol 22:976–990PubMedCrossRefGoogle Scholar
  72. Shpiz S, Kwon D, Uneva A et al (2007) Characterization of Drosophila telomeric retroelement TAHRE: transcription, transpositions, and RNAi-based regulation of expression. Mol Biol Evol 24:2535–2545PubMedCrossRefGoogle Scholar
  73. Simmons MJ, Ryzek DF, Lamour C et al (2007) Cytotype regulation by telomeric P elements in Drosophila melanogaster: evidence for involvement of an RNA interference gene. Genetics 176:1945–1955PubMedCrossRefGoogle Scholar
  74. Slotkin KR, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8:272–285PubMedCrossRefGoogle Scholar
  75. Slotkin RK, Freeling M, Lisch D (2003) Mu killer causes the heritable inactivation of the Mutator family of transposable elements in Zea mays. Genetics 165:781–797PubMedGoogle Scholar
  76. Slotkin RK, Freeling M, Lisch D (2005) Heritable transposon silencing initiated by a naturally occurring transposon inverted duplication. Nat Genet 37:641–644PubMedCrossRefGoogle Scholar
  77. Slotkin KR, Vaughn M, Borges F (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–472PubMedCrossRefGoogle Scholar
  78. Staton SE, Ungerer MC, Moore RC (2009) The genomic organization of Ty3/Gypsy-like retrotransposons in Helianthus (Asteraceae) homoploid hybrid species. Am J Bot 96:1646–1655PubMedCrossRefGoogle Scholar
  79. Tenaillon MI, Hollister JD, Gaut BS (2010) A triptych of the evolution of plant transposable elements. Trends Plant Sci 15:471–478PubMedCrossRefGoogle Scholar
  80. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefGoogle Scholar
  81. Ungerer MC, Strakosh SC, Zhen Y (2006) Genome expansion in three hybrid sunflower species is associated with retrotransposon proliferation. Curr Biol 16:872–873CrossRefGoogle Scholar
  82. Vitte C, Panaud O (2005) LTR retrotransposons and flowering plant genome size: emergence of the increase/decrease model. Cytogenet Genome Res 110:91–107PubMedCrossRefGoogle Scholar
  83. Vu W, Nuzhdin S (2011) Genetic variation of copia suppression in Drosophila melanogaster. Heredity 106:207–217PubMedCrossRefGoogle Scholar
  84. Wang NN, Wang HY, Wang H et al (2010) Transpositoinal reactivation of the Dart transposon family in rice lines derived from introgressive hybridization with Zizania latifolia. BMC Plant Biol 10:190PubMedCrossRefGoogle Scholar
  85. Waugh O'Neill RJ, O'Neill MJ, Marshall Graves JA (1998) Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 393:68–72CrossRefGoogle Scholar
  86. Whitney KD, Garland T Jr (2010) Did genetic drift drive increases in genome complexity? PLoS Genet 6:e1001080. doi: 10.1371/journal.pgen.1001080 PubMedCrossRefGoogle Scholar
  87. Whitney KD, Baack EJ, Hamrick JL et al (2010) A role for nonadtive processes in plant genome evolution? Evolution 64:2097–2109PubMedGoogle Scholar
  88. Whitney KD, Boussau B, Baack EJ, Garland T Jr (2011) Drift and genome complexity revisited. PLoS Genet 7:e1002092. doi: 10.1371/journal.pgen.1002092 PubMedCrossRefGoogle Scholar
  89. Wicker T, Guyot R, Yahiaoui N (2003) CACTA transposons in Triticeae—a diverse family of high-copy repetitive elements. Plant Physiol 132:52–63PubMedCrossRefGoogle Scholar
  90. Wicker T, Zimmerman W, Perovic D et al (2005) A detailed look at 7 million years of genome evolution in 439 kb contiguous barley Hv-elF4E locus: recombination, rearrangements and repeats. Plant J 41:184–194PubMedCrossRefGoogle Scholar
  91. Wright S, Finnegan D (2001) Genome evolution: sex and transposable element. Curr Biol 11:R296–R299PubMedCrossRefGoogle Scholar
  92. Wright SI, Schoen DJ (1999) Transposon dynamic and the breeding system. Genetica 107:139–148PubMedCrossRefGoogle Scholar
  93. Wright SI, Le QH, Schoen DJ et al (2001) Population dynamics of an Ac-like transposable element in self- and cross-pollinating Arabidopsis. Genetics 158:1279–1288PubMedGoogle Scholar
  94. Wright SI, Ness RW, Foxe JP, Barrett SCH (2008) Genomic consequences of outcrossing and selfing in plants. Int J Plant Sci 169:105–118CrossRefGoogle Scholar
  95. Yang GJ, Nagel DN, Feschotte C, Hancock NC, Wessler SR (2009) Tuned for transposition: molecular determinants underlying the hyperactivity of a stowaway MITE. Science 325:1391–1394PubMedCrossRefGoogle Scholar
  96. Zhang X (2008) The epigenetic landscape of plants. Science 320:489–492PubMedCrossRefGoogle Scholar
  97. Zilberman D, Henikoff S (2007) Genome-wide analysis of DNA methylation patterns. Development 134:3959–3965PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of TorontoTorontoCanada

Personalised recommendations