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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McClintock, B. The significance of responses of the genome to challenge. Science 226, 792–801 (1984)
Ries, G. et al. Elevated UV-B radiation reduces genome stability in plants. Nature 406, 98–101 (2000)
Lucht, J. M. et al. Pathogen stress increases somatic recombination frequency in Arabidopsis. Nature Genet. 30, 311–314 (2002)
Kovalchuk, I. et al. Pathogen-induced systemic plant signal triggers DNA rearrangements. Nature 423, 760–762 (2003)
Cullis, C. A. Mechanisms and control of rapid genomic changes in flax. Ann. Bot. (Lond.) 95, 201–206 (2005)
Zipfel, C. et al. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428, 764–767 (2004)
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)
Walbot, V. Reactivation of Mutator transposable elements of maize by ultraviolet light. Mol. Gen. Genet. 234, 353–360 (1992)
Grandbastien, M. A. et al. Stress activation and genomic impact of Tnt1 retrotransposons in Solanaceae. Cytogenet. Genome Res. 110, 229–241 (2005)
Kovalchuk, I., Kovalchuk, O. & Hohn, B. Genome-wide variation of the somatic mutation frequency in transgenic plants. EMBO J. 19, 4431–4438 (2000)
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)
Walbot, V. Sources and consequences of phenotypic plasticity in flowering plants. Trends Plant Sci. 1, 27–32 (1996)
Swoboda, P., Gal, S., Hohn, B. & Puchta, H. Intrachromosomal homologous recombination in whole plants. EMBO J. 13, 484–489 (1994)
Molinier, J., Ries, G., Bonhoeffer, S. & Hohn, B. Interchromatid and interhomolog recombination in Arabidopsis thaliana. Plant Cell 16, 342–352 (2004)
Schuermann, D., Molinier, J., Fritsch, O. & Hohn, B. The dual nature of homologous recombination in plants. Trends Genet. 21, 172–181 (2005)
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)
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)
Puchta, H., Swoboda, P. & Hohn, B. Induction of intrachromosomal homologous recombination in whole plants. Plant J. 7, 203–210 (1995)
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)
Madlung, A. & Comai, L. The effect of stress on genome regulation and structure. Ann. Bot. (Lond.) 94, 481–495 (2004)
Cubas, P., Vincent, C. & Coen, E. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401, 157–161 (1999)
Jacobsen, S. & Meyerowitz, E. M. Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277, 1100–1103 (1997)
Jablonka, E. & Lamb, M. J. Epigenetic Inheritance and Evolution: The Lamarckian Dimension (Oxford Univ. Press, Oxford, 1995)
Gherbi, H. et al. Homologous recombination in planta is stimulated in the absence of Rad50. EMBO Rep. 2, 287–291 (2001)
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)
Jefferson, R. A. Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol. Biol. Rep. 5, 387–405 (1987)
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.
Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.
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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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