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In Arabidopsis mutants compromised in 24-nucleotide siRNA biogenesis, transposon transcripts appear but transposition has not been observed (3,4). This is in contrast to mutants lacking chromatin- remodelling factor DDM1 or [...], Eukaryotic genomes consist to a significant extent of retrotransposons that are suppressed by host epigenetic mechanisms, preventing their uncontrolled propagation (1,2). However, it is not clear how this is achieved. Here we show that in Arabidopsis seedlings subjected to heat stress, a copia-type retrotransposon named ONSEN (Japanese 'hot spring') not only became transcriptionally active but also synthesized extrachromosomal DNA copies. Heat-induced ONSEN accumulation was stimulated in mutants impaired in the biogenesis of small interfering RNAs (siRNAs); however, there was no evidence of transposition occurring in vegetative tissues. After stress, both ONSEN transcripts and extrachromosomal DNA gradually decayed and were no longer detected after 20-30 days. Surprisingly, a high frequency of new ONSEN insertions was observed in the progeny of stressed plants deficient in siRNAs. Insertion patterns revealed that this transgenerational retrotransposition occurred during flower development and before gametogenesis. Therefore in plants with compromised siRNA biogenesis, memory of stress was maintained throughout development, priming ONSEN to transpose during differentiation of generative organs. Retrotransposition was not observed in the progeny of wild-type plants subjected to stress or in non-stressed mutant controls, pointing to a crucial role of the siRNA pathway in restricting retrotransposition triggered by environmental stress. Finally, we found that natural and experimentally induced variants in ONSEN insertions confer heat responsiveness to nearby genes, and therefore mobility bursts may generate novel, stress-responsive regulatory gene networks.

We established a population of epigenetic recombinant inbred lines (epiRILs) derived from a cross between a wild-type (WT) and a metl homozygous plant carrying a null mutation for METI (metl [...], Retrotransposons are mobile genetic elements that populate chromosomes, where the host largely controls their activities (1-3). In plants and mammals, retrotransposons are transcriptionally silenced by DNA methylation (1,4), which in Arabidopsis is propagated at CG dinucleotides by METHYLTRANSFERASE 1 (METl)s. In metl mutants, however, mobilization of retrotransposons is not observed, despite their transcriptional activation (4-6). A posttranscriptional mechanism therefore seems to be preventing retrotransposition. Here we show that a copia-type retrotransposon (Evade, French for 'fugitive') evaded suppression of its movement during inbreeding of hybrid epigenomes consisting of metl- and wild-type-derived chromosomes. Evade (EVD) reinsertions caused a series of developmental mutations that allowed its identification. Genetic testing of host control of the EVD life cycle showed that transcriptional suppression occurred by CG methylation supported by RNA-directed DNA methylation. On transcriptional reactivation, subsequent steps of the EVD rycle were inhibited by plant-specific RNA polymerase IV/V (7,8) and the histone methyltransferase KRYPTONITE (KYP). Moreover, genome resequencing demonstrated retrotransposition of EVD but no other potentially active retroelements when this combination of epigenetic mechanisms was compromised. Our results demonstrate that epigenetic control of retrotransposons extends beyond transcriptional suppression and can be individualized for particular elements.