Abstract
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
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Kumar, A. & Bennetzen, J. L. Plant retrotransposons. Annu. Rev. Genet. 33, 479–532 (1999)
Havecker, E. R., Gao, X. & Voytas, D. F. The diversity of LTR retrotransposons. Genome Biol. 5, 225 (2004)
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)
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)
The Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana . Nature 408, 796–815 (2000)
Le, Q. H., Wright, S., Yu, Z. & Bureau, T. Transposon diversity in Arabidopsis thaliana . Proc. Natl Acad. Sci. USA 97, 7376–7381 (2000)
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)
Steimer, A. et al. Endogenous targets of transcriptional gene silencing in Arabidopsis . Plant Cell 12, 1165–1178 (2000)
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)
Vongs, A., Kakutani, T., Martienssen, R. A. & Richards, E. J. Arabidopsis thaliana DNA methylation mutants. Science 260, 1926–1928 (1993)
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)
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)
Hirochika, H., Okamoto, H. & Kakutani, T. Silencing of retrotransposons in Arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12, 357–369 (2000)
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)
Bender, J. DNA methylation and epigenetics. Annu. Rev. Plant Biol. 55, 41–68 (2004)
Chan, S. W., Henderson, I. R. & Jacobsen, S. E. Gardening the genome: DNA methylation in Arabidopsis thaliana . Nature Rev. Genet. 6, 351–360 (2005)
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)
Miura, A. et al. Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis . Nature 411, 212–214 (2001)
Kakutani, T. Genetic characterization of late-flowering traits induced by DNA hypomethylation mutation in Arabidopsis thaliana . Plant J. 12, 1447–1451 (1997)
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)
Cokus, S. J. et al. Shotgun bisulfite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452, 215–219 (2008)
Lister, R. et al. Highly integrated single-base resolution maps of epigenome in Arabidopsis . Cell 133, 523–536 (2008)
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)
Yu, Z., Wright, S. I. & Bureau, T. E. Mutator-like elements in Arabidopsis thaliana: structure, diversity and evolution. Genetics 156, 2019–2031 (2000)
Mirouze, M. et al. Selective epigenetic control of retrotransposition in Arabidopsis . Nature 10.1038/nature08328 (this issue)
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)
Kankel, M. W. et al. Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163, 1109–1122 (2003)
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)
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)
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)
Acknowledgements
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
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)
Rights 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). https://doi.org/10.1038/nature08351
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature08351
This article is cited by
-
From parasites to partners: exploring the intricacies of host-transposon dynamics and coevolution
Functional & Integrative Genomics (2023)
-
Transposable element finder (TEF): finding active transposable elements from next generation sequencing data
BMC Bioinformatics (2022)
-
The fifth Japanese meeting on biological function and evolution through interactions between hosts and transposable elements
Mobile DNA (2022)
-
Manipulating base quality scores enables variant calling from bisulfite sequencing alignments using conventional bayesian approaches
BMC Genomics (2022)
-
DNA methylation-free Arabidopsis reveals crucial roles of DNA methylation in regulating gene expression and development
Nature Communications (2022)
Comments
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.