1. Department of Integrated Genetics, National Institute of Genetics, Yata 1111, Mishima, Shizuoka 411-8540, Japan
2. Department of Genetics, School of Life Science, The Graduate University for Advanced Studies, Yata 1111, Mishima, Shizuoka 411-8540, Japan
3. Department of Plant Biology, University of Geneva, Sciences III, 30 Quai Ernest-Ansermet, CH-1211 Geneva 4, Switzerland
4. Centre National de la Recherche Scientifique (CNRS), UMR 6247, GReD, INSERM U 931, Clermont Université, 24 avenue des landais, 63177 Aubière, France
5. These authors contributed equally to this work.

Correspondence to: Tetsuji Kakutani^1,2 Correspondence and requests for materials should be addressed to T.K. (Email: tkakutan@lab.nig.ac.jp).

Abstract

Retrotransposons, which proliferate by reverse transcription of RNA intermediates, comprise a major portion of plant genomes^{1, 2}. Plants often change the genome size and organization during evolution by rapid proliferation and deletion of long terminal repeat (LTR) retrotransposons^{3, 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 dynamics^{5, 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.