Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Bursts of retrotransposition reproduced in Arabidopsis


Retrotransposons, which proliferate by reverse transcription of RNA intermediates, comprise a major portion of plant genomes1,2. Plants often change the genome size and organization during evolution by rapid proliferation and deletion of long terminal repeat (LTR) retrotransposons3,4. Precise transposon sequences throughout the Arabidopsis thaliana genome and the trans-acting mutations affecting epigenetic states make it an ideal model organism with which to study transposon dynamics5,6,7,8,9. Here we report the mobilization of various families of endogenous A. thaliana LTR retrotransposons identified through genetic and genomic approaches with high-resolution genomic tiling arrays and mutants in the chromatin-remodelling gene DDM1 (DECREASE IN DNA METHYLATION 1)10,11. Using multiple lines of self-pollinated ddm1 mutant, we detected an increase in copy number, and verified this for various retrotransposons in a gypsy family (ATGP3) and copia families (ATCOPIA13, ATCOPIA21, ATCOPIA93), and also for a DNA transposon of a Mutator family, VANDAL21. A burst of retrotransposition occurred stochastically and independently for each element, suggesting an additional autocatalytic process. Furthermore, comparison of the identified LTR retrotransposons in related Arabidopsis species revealed that a lineage-specific burst of retrotransposition of these elements did indeed occur in natural Arabidopsis populations. The recent burst of retrotransposition in natural population is targeted to centromeric repeats, which is presumably less harmful than insertion into genes. The ddm1-induced retrotransposon proliferations and genome rearrangements mimic the transposon-mediated genome dynamics during evolution and provide experimental systems with which to investigate the controlling molecular factors directly.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Identification of a mobile gypsy element ATGP3 through characterization of a ddm1 -induced developmental phenotype.
Figure 2: Increases in copy number in transposons can be detected with a genomic tiling array.
Figure 3: Lineage-specific bursts of retrotransposition.
Figure 4: Selective integration of COPIA93 into centromeric satellite repeats of the A. lyrata genome.


  1. Kumar, A. & Bennetzen, J. L. Plant retrotransposons. Annu. Rev. Genet. 33, 479–532 (1999)

    CAS  Article  Google Scholar 

  2. Havecker, E. R., Gao, X. & Voytas, D. F. The diversity of LTR retrotransposons. Genome Biol. 5, 225 (2004)

    Article  Google Scholar 

  3. Vitte, C. & Bennetzen, J. L. Analysis of retrotransposon structural diversity uncovers properties and propensities in angiosperm genome evolution. Proc. Natl Acad. Sci. USA 103, 17638–17643 (2006)

    ADS  CAS  Article  Google Scholar 

  4. Hawkins, J. S., Kim, H. & Nason, J. D. Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium . Genome Res. 16, 1252–1261 (2006)

    CAS  Article  Google Scholar 

  5. The Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana . Nature 408, 796–815 (2000)

  6. Le, Q. H., Wright, S., Yu, Z. & Bureau, T. Transposon diversity in Arabidopsis thaliana . Proc. Natl Acad. Sci. USA 97, 7376–7381 (2000)

    ADS  CAS  Article  Google Scholar 

  7. Peterson-Burch, B. D., Nettleton, D. & Voytas, D. F. Genomic neighborhoods for Arabidopsis retrotransposons: a role for targeted integration in the distribution of the Metaviridae. Genome Biol. 5, R78 (2004)

    Article  Google Scholar 

  8. Steimer, A. et al. Endogenous targets of transcriptional gene silencing in Arabidopsis . Plant Cell 12, 1165–1178 (2000)

    CAS  Article  Google Scholar 

  9. Lippman, Z., May, B., Yordan, C., Singer, T. & Martienssen, R. Distinct mechanisms to determine transposon inheritance and methylation via small interfering RNA and histone modification. PLoS Biol. 1, E67 (2003)

    Article  Google Scholar 

  10. Vongs, A., Kakutani, T., Martienssen, R. A. & Richards, E. J. Arabidopsis thaliana DNA methylation mutants. Science 260, 1926–1928 (1993)

    ADS  CAS  Article  Google Scholar 

  11. Jeddeloh, J. A., Stokes, T. L. & Richards, E. J. Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nature Genet. 22, 94–97 (1999)

    CAS  Article  Google Scholar 

  12. Lucas, H., Feuerbach, F., Kunert, K., Grandbastien, M.-A. & Caboche, M. RNA-mediated transposition of the tobacco retrotransposon Tnt1 in Arabidopsis thaliana . EMBO J. 14, 2364–2373 (1995)

    CAS  Article  Google Scholar 

  13. Hirochika, H., Okamoto, H. & Kakutani, T. Silencing of retrotransposons in Arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12, 357–369 (2000)

    CAS  Article  Google Scholar 

  14. Finnegan, E., Peacock, J. & Dennis, E. Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc. Natl Acad. Sci. USA 93, 8449–8454 (1996)

    ADS  CAS  Article  Google Scholar 

  15. Bender, J. DNA methylation and epigenetics. Annu. Rev. Plant Biol. 55, 41–68 (2004)

    CAS  Article  Google Scholar 

  16. Chan, S. W., Henderson, I. R. & Jacobsen, S. E. Gardening the genome: DNA methylation in Arabidopsis thaliana . Nature Rev. Genet. 6, 351–360 (2005)

    CAS  Article  Google Scholar 

  17. Kakutani, T., Jeddeloh, J., Flowers, S., Munakata, K. & Richards, E. Developmental abnormalities and epimutations associated with DNA hypomethylation mutations. Proc. Natl Acad. Sci. USA 93, 12406–12411 (1996)

    ADS  CAS  Article  Google Scholar 

  18. Miura, A. et al. Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis . Nature 411, 212–214 (2001)

    ADS  CAS  Article  Google Scholar 

  19. Kakutani, T. Genetic characterization of late-flowering traits induced by DNA hypomethylation mutation in Arabidopsis thaliana . Plant J. 12, 1447–1451 (1997)

    CAS  Article  Google Scholar 

  20. Kaya, H. et al. FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 104, 131–142 (2001)

    CAS  Article  Google Scholar 

  21. Cokus, S. J. et al. Shotgun bisulfite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452, 215–219 (2008)

    ADS  CAS  Article  Google Scholar 

  22. Lister, R. et al. Highly integrated single-base resolution maps of epigenome in Arabidopsis . Cell 133, 523–536 (2008)

    CAS  Article  Google Scholar 

  23. Singer, T., Yordan, C. & Martienssen, R. A. Robertson’s Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1). Genes Dev. 15, 591–602 (2001)

    CAS  Article  Google Scholar 

  24. Yu, Z., Wright, S. I. & Bureau, T. E. Mutator-like elements in Arabidopsis thaliana: structure, diversity and evolution. Genetics 156, 2019–2031 (2000)

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Mirouze, M. et al. Selective epigenetic control of retrotransposition in Arabidopsis . Nature 10.1038/nature08328 (this issue)

  26. Kawabe, A. & Charlesworth, D. Patterns of DNA variation among three centromere satellite families in Arabidopsis halleri and A. lyrata . J. Mol. Evol. 64, 237–247 (2007)

    ADS  CAS  Article  Google Scholar 

  27. Kankel, M. W. et al. Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163, 1109–1122 (2003)

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Bartee, L., Malagnac, F. & Bender, J. Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Genes Dev. 15, 1753–1758 (2001)

    CAS  Article  Google Scholar 

  29. Kato, M., Miura, A., Bender, J., Jacobsen, S. & Kakutani, T. Role of CG and non-CG methylation in immobilization of transposons in Arabidopsis . Curr. Biol. 13, 421–426 (2003)

    CAS  Article  Google Scholar 

  30. Tamura, K., Dudley, J., Nei, M. & Kumar, S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596–1599 (2007)

    CAS  Article  Google Scholar 

Download references


We thank A. Terui for technical assistance, M. Nakamura for plant materials, M. Morita and M. Tasaka for genetic marker information, H. Tsukaya for advice on the wvs phenotypes, and E. Richards for critical comments on the manuscript. This study was supported by the Takeda Science Foundation and a Grant-in-Aid for Scientific Research.

Author Contributions S.T. identified and analysed ATGP3. A. Kobayashi collected and analysed tiling array data. A.M., S.T., A. Kobayashi and T.K. performed the Southern blot analysis. O.M. obtained the results shown in Supplementary Fig. 6, and A. Kawabe analysed the sequences. S.T. and T.K. wrote the manuscript. All authors discussed and commented on the manuscript.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Tetsuji Kakutani.

Supplementary information

Supplementary information

This file contains Supplementary Figures 1-9 with Legends, a Supplementary Discussion, Supplementary References, Supplementary Tables 1-4 and Supplementary Sequence Data. (PDF 6167 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Tsukahara, S., Kobayashi, A., Kawabe, A. et al. Bursts of retrotransposition reproduced in Arabidopsis. Nature 461, 423–426 (2009).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing