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An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress

Abstract

Eukaryotic genomes consist to a significant extent of retrotransposons that are suppressed by host epigenetic mechanisms, preventing their uncontrolled propagation1,2. 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.

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Figure 1: Heat-stress induced ONSEN transcription.
Figure 2: Accumulation of ONSEN extrachromosomal DNA.
Figure 3: Burst of ONSEN transposition in the progeny of HS-treated nrpd1 plants.
Figure 4: Acquisition of heat-responsive transcription by ONSEN -containing loci and model of ONSEN activation.

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Acknowledgements

We thank all members of the J.P. laboratory and R. L. Fisher for discussions, L. Broger, M. Freyre, J. Nicolet, C. Mégies for technical assistance and P. King and J. Reinders for editing of the manuscript. This work was supported by grants from the Swiss National Science Foundation (31003A-125005) and the European Commission through the AENEAS collaborative project (FP7 226477), the RECBREED consortium (FP7 227190) and The Epigenome Network of Excellence (FP6 503433).

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H.I., E.B., H.G., M.M. and J.P. conceived the study. H.I., E.B., H.G., M.M. and I.V. performed the experiments. J.P. wrote the paper with contributions from E.B. and M.M.

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Correspondence to Jerzy Paszkowski.

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The authors declare no competing financial interests.

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Ito, H., Gaubert, H., Bucher, E. et al. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472, 115–119 (2011). https://doi.org/10.1038/nature09861

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