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Transgeneration memory of stress in plants

Nature volume 442, pages 1046–1049 (2006)Cite this article

Abstract

Owing to their sessile nature, plants are constantly exposed to a multitude of environmental stresses to which they react with a battery of responses. The result is plant tolerance to conditions such as excessive or inadequate light, water, salt and temperature, and resistance to pathogens. Not only is plant physiology known to change under abiotic or biotic stress, but changes in the genome have also been identified1,2,3,4,5. However, it was not determined whether plants from successive generations of the original, stressed plants inherited the capacity for genomic change. Here we show that in Arabidopsis thaliana plants treated with short-wavelength radiation (ultraviolet-C) or flagellin (an elicitor of plant defences6), somatic homologous recombination of a transgenic reporter is increased in the treated population and these increased levels of homologous recombination persist in the subsequent, untreated generations. The epigenetic trait of enhanced homologous recombination could be transmitted through both the maternal and the paternal crossing partner, and proved to be dominant. The increase of the hyper-recombination state in generations subsequent to the treated generation was independent of the presence of the transgenic allele (the recombination substrate under consideration) in the treated plant. We conclude that environmental factors lead to increased genomic flexibility even in successive, untreated generations, and may increase the potential for adaptation.

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Figure 1: Somatic homologous recombination in UV-C- and flg22-treated plants.
Figure 2: Somatic HRF in S 0 lines and their respective S 1 progenies.
Figure 3: Somatic HRF in S0 plants and in the next four generations. S0 plants (line IC1) were either untreated or UV-treated.
Figure 4: Somatic HRF in either self-pollinated or outcrossed plants.

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References

  1. McClintock, B. The significance of responses of the genome to challenge. Science 226, 792–801 (1984)

    Article  ADS  CAS  Google Scholar 

  2. Ries, G. et al. Elevated UV-B radiation reduces genome stability in plants. Nature 406, 98–101 (2000)

    Article  ADS  CAS  Google Scholar 

  3. Lucht, J. M. et al. Pathogen stress increases somatic recombination frequency in Arabidopsis. Nature Genet. 30, 311–314 (2002)

    Article  Google Scholar 

  4. Kovalchuk, I. et al. Pathogen-induced systemic plant signal triggers DNA rearrangements. Nature 423, 760–762 (2003)

    Article  ADS  CAS  Google Scholar 

  5. Cullis, C. A. Mechanisms and control of rapid genomic changes in flax. Ann. Bot. (Lond.) 95, 201–206 (2005)

    Article  CAS  Google Scholar 

  6. Zipfel, C. et al. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428, 764–767 (2004)

    Article  ADS  CAS  Google Scholar 

  7. Mottinger, J. P., Johns, M. A. & Freeling, M. Mutations of the Adh1 gene in maize following infection with barley stripe mosaic virus. Mol. Gen. Genet. 195, 367–369 (1984)

    Article  CAS  Google Scholar 

  8. Walbot, V. Reactivation of Mutator transposable elements of maize by ultraviolet light. Mol. Gen. Genet. 234, 353–360 (1992)

    Article  CAS  Google Scholar 

  9. Grandbastien, M. A. et al. Stress activation and genomic impact of Tnt1 retrotransposons in Solanaceae. Cytogenet. Genome Res. 110, 229–241 (2005)

    Article  CAS  Google Scholar 

  10. Kovalchuk, I., Kovalchuk, O. & Hohn, B. Genome-wide variation of the somatic mutation frequency in transgenic plants. EMBO J. 19, 4431–4438 (2000)

    Article  CAS  Google Scholar 

  11. Lebel, E. G., Masson, J., Bogucki, A. & Paszkowski, J. Stress-induced intrachromosomal recombination in plant somatic cells. Proc. Natl Acad. Sci. USA 90, 422–426 (1993)

    Article  ADS  CAS  Google Scholar 

  12. Walbot, V. Sources and consequences of phenotypic plasticity in flowering plants. Trends Plant Sci. 1, 27–32 (1996)

    Article  Google Scholar 

  13. Swoboda, P., Gal, S., Hohn, B. & Puchta, H. Intrachromosomal homologous recombination in whole plants. EMBO J. 13, 484–489 (1994)

    Article  CAS  Google Scholar 

  14. Molinier, J., Ries, G., Bonhoeffer, S. & Hohn, B. Interchromatid and interhomolog recombination in Arabidopsis thaliana. Plant Cell 16, 342–352 (2004)

    Article  CAS  Google Scholar 

  15. Schuermann, D., Molinier, J., Fritsch, O. & Hohn, B. The dual nature of homologous recombination in plants. Trends Genet. 21, 172–181 (2005)

    Article  CAS  Google Scholar 

  16. Felix, G., Duran, J. D., Volko, S. & Boller, T. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18, 265–276 (1999)

    Article  CAS  Google Scholar 

  17. Klumpp, A., Ansel, W., Fomin, A., Schnirring, S. & Pickl, C. Influence of climatic conditions on the mutations in pollen mother cells of Tradescantia clone 4430 and implications for the Trad-MCN bioassay protocol. Hereditas 141, 142–148 (2004)

    Article  Google Scholar 

  18. Puchta, H., Swoboda, P. & Hohn, B. Induction of intrachromosomal homologous recombination in whole plants. Plant J. 7, 203–210 (1995)

    Article  CAS  Google Scholar 

  19. Jorgensen, R. A. Restructuring the genome in response to adaptive challenge: McClintock's bold conjecture revisited. Cold Spring Harb. Symp. Quant. Biol. 69, 349–354 (2004)

    Article  CAS  Google Scholar 

  20. Madlung, A. & Comai, L. The effect of stress on genome regulation and structure. Ann. Bot. (Lond.) 94, 481–495 (2004)

    Article  CAS  Google Scholar 

  21. Cubas, P., Vincent, C. & Coen, E. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401, 157–161 (1999)

    Article  ADS  CAS  Google Scholar 

  22. Jacobsen, S. & Meyerowitz, E. M. Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277, 1100–1103 (1997)

    Article  CAS  Google Scholar 

  23. Jablonka, E. & Lamb, M. J. Epigenetic Inheritance and Evolution: The Lamarckian Dimension (Oxford Univ. Press, Oxford, 1995)

    Google Scholar 

  24. Gherbi, H. et al. Homologous recombination in planta is stimulated in the absence of Rad50. EMBO Rep. 2, 287–291 (2001)

    Article  CAS  Google Scholar 

  25. Puchta, H., Swoboda, P., Gal, S., Blot, M. & Hohn, B. Somatic intrachromosomal recombination events in populations of plant siblings. Plant Mol. Biol. 28, 281–292 (1995)

    Article  CAS  Google Scholar 

  26. Jefferson, R. A. Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol. Biol. Rep. 5, 387–405 (1987)

    Article  CAS  Google Scholar 

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Acknowledgements

We acknowledge the critical analysis of the manuscript by O. M. Scheid, D. Schuermann, R. Jorgensen, U. Grossniklaus, D. Schuebeler, L. Comai and T. Boller. We are grateful to the Novartis Research Foundation and the European Union project PLANTREC for financial support.

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Author notes

  1. Jean Molinier

    Present address: Institut de Biologie Moléculaire des Plantes, 12 Rue du Général Zimmer, F-67084, Strasbourg Cedex, France

  2. Gerhard Ries

    Present address: BioMedinvestor AG, Elisabethenstrasse 23, CH-4051, Basel, Switzerland

  3. Cyril Zipfel

    Present address: The Sainsbury Laboratory, John Innes Centre, Colney Lane, Norwich, NR4 7UH, UK

Authors and Affiliations

  1. Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, CH-4058, Basel, Switzerland

    Jean Molinier, Gerhard Ries, Cyril Zipfel & Barbara Hohn

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  1. Jean Molinier
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Correspondence to Barbara Hohn.

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Molinier, J., Ries, G., Zipfel, C. et al. Transgeneration memory of stress in plants. Nature 442, 1046–1049 (2006). https://doi.org/10.1038/nature05022

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