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Bursts of retrotransposition reproduced in Arabidopsis

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.

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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.

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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.

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Correspondence to Tetsuji Kakutani.

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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)

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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

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