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An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress

Nature volume 472, pages 115–119 (2011)Cite this article

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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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References

  1. Slotkin, R. K. & Martienssen, R. Transposable elements and the epigenetic regulation of the genome. Nature Rev. Genet. 8, 272–285 (2007)

    Article  CAS  Google Scholar 

  2. Lisch, D. Epigenetic regulation of transposable elements in plants. Annu. Rev. Plant Biol. 60, 43–66 (2008)

    Article  Google Scholar 

  3. Herr, A. J., Jensen, M. B., Dalmay, T. & Baulcombe, D. C. RNA polymerase IV directs silencing of endogenous DNA. Science 308, 118–120 (2005)

    Article  ADS  CAS  Google Scholar 

  4. Mosher, R. A., Schwach, F., Studholme, D. & Baulcombe, D. C. PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis. Proc. Natl Acad. Sci. USA 105, 3145–3150 (2008)

    Article  ADS  CAS  Google Scholar 

  5. Miura, A. et al. Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis . Nature 411, 212–214 (2001)

    Article  ADS  CAS  Google Scholar 

  6. Tsukahara, S. et al. Bursts of retrotransposition reproduced in Arabidopsis . Nature 461, 423–426 (2009)

    Article  ADS  CAS  Google Scholar 

  7. Johannes, F. et al. Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet. 5, e1000530 (2009)

    Article  Google Scholar 

  8. Reinders, J. et al. Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev. 23, 939–950 (2009)

    Article  CAS  Google Scholar 

  9. Mirouze, M. et al. Selective epigenetic control of retrotransposition in Arabidopsis . Nature 461, 427–430 (2009)

    Article  ADS  CAS  Google Scholar 

  10. Slotkin, R. K. et al. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136, 461–472 (2009)

    Article  CAS  Google Scholar 

  11. Mosher, R. A. et al. Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis . Nature 460, 283–286 (2009)

    Article  ADS  CAS  Google Scholar 

  12. Hsieh, T.-F. et al. Genome-wide demethylation of Arabidopsis endosperm. Science 324, 1451–1454 (2009)

    Article  ADS  CAS  Google Scholar 

  13. Gehring, M., Bubb, K. L. & Henikoff, S. Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324, 1447–1451 (2009)

    Article  ADS  CAS  Google Scholar 

  14. Tittel-Elmer, M. et al. Stress-induced activation of heterochromatic transcription. PLoS Genet. 6, e1001175 (2010)

    Article  Google Scholar 

  15. Pecinka, A. et al. Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis . Plant Cell 22, 3118–3129 (2010)

    Article  CAS  Google Scholar 

  16. Hirochika, H., Okamoto, H. & Kakutani, T. Silencing of retrotransposons in Arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12, 357–369 (2000)

    Article  CAS  Google Scholar 

  17. Onodera, Y. et al. Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120, 613–622 (2005)

    Article  CAS  Google Scholar 

  18. Xie, Z. et al. Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2, e104 (2004)

    Article  Google Scholar 

  19. Naumann, K. et al. Pivotal role of AtSUVH2 in heterochromatic histone methylation and gene silencing in Arabidopsis . EMBO J. 24, 1418–1429 (2005)

    Article  CAS  Google Scholar 

  20. Feuerbach, F., Drouaud, J. & Lucas, H. Retrovirus-like end processing of the tobacco Tnt1 retrotransposon linear intermediates of replication. J. Virol. 71, 4005–4015 (1997)

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Hirochika, H. & Otsuki, H. Extrachromosomal circular forms of the tobacco retrotransposon Tto1 . Gene 165, 229–232 (1995)

    Article  CAS  Google Scholar 

  22. Johnson, L. M., Law, J. A., Khattar, A., Henderson, I. R. & Jacobsen, S. E. SRA-domain proteins required for DRM2-mediated de novo DNA methylation. PLoS Genet. 4, e1000280 (2008)

    Article  Google Scholar 

  23. Law, J. A. & Jacobsen, S. E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Rev. Genet. 11, 204–220 (2010)

    Article  CAS  Google Scholar 

  24. Vaucheret, H. Plant ARGONAUTES. Trends Plant Sci. 13, 350–358 (2008)

    Article  CAS  Google Scholar 

  25. Vagin, V. V. et al. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313, 320–324 (2006)

    Article  ADS  CAS  Google Scholar 

  26. Piegu, B. et al. Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res. 16, 1262–1269 (2006)

    Article  CAS  Google Scholar 

  27. Ammiraju, J. S. S. et al. Evolutionary dynamics of an ancient retrotransposon family provides insights into evolution of genome size in the genus Oryza . Plant J. 52, 342–351 (2007)

    Article  CAS  Google Scholar 

  28. Naito, K. et al. Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461, 1130–1134 (2009)

    Article  ADS  CAS  Google Scholar 

  29. Lim, C. J. et al. Gene expression profiles during heat acclimation in Arabidopsis thaliana suspension-culture cells. J. Plant Res. 119, 373–383 (2006)

    Article  CAS  Google Scholar 

  30. Vongs, A., Kakutani, T., Martienssen, R. A. & Richards, E. J. Arabidopsis thaliana DNA methylation mutants. Science 260, 1926–1928 (1993)

    Article  ADS  CAS  Google Scholar 

Download references

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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  1. Hidetaka Ito, Etienne Bucher, Marie Mirouze & Isabelle Vaillant

    Present address: Present addresses: Division of Biological Sciences, Graduate School of Science, Hokkaido University, 060-0810 Sapporo, Japan (H.I.); Botanical Institute, Hebelstrasse 1, CH-4056 Basel, Switzerland (E.B.); Institut de Recherche pour le Développement (IRD), UMR DIADE, Plant Diversity, Adaptation and Development Laboratory, Université Montpellier 2, 911 Avenue Agropolis, 34394 Montpellier, France (M.M.); Centre National de la Recherche Scientifique (CNRS), UMR 6247 - GReD - INSERM U 931, Clermont Université, 24 avenue des Landais, BP 80026, 63171 Aubière, France (I.V.).,

  2. Hidetaka Ito, Hervé Gaubert and Etienne Bucher: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Plant Biology, University of Geneva, Sciences III, 30 Quai Ernest-Ansermet, CH-1211 Geneva 4, Switzerland

    Hidetaka Ito, Hervé Gaubert, Etienne Bucher, Marie Mirouze, Isabelle Vaillant & Jerzy Paszkowski

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  1. Hidetaka Ito
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Contributions

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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