Environmental stressors induce epigenetic changes that plants pass to their progeny
By Melissa Lee Phillips | August 7, 2006
Plants can pass on "memories" of stress to their offspring, possibly helping them adapt to their environments, according to a study published online in Nature this week. The researchers found that the progeny of plants exposed to UV radiation or a bacterial protein showed the same genomic instability that their parents did, even though offspring didn't experience either stressor.
"Stress causing something to be inherited is really quite novel," said Steven Henikoff of the Fred Hutchinson Cancer Research Center in Seattle, who was not involved in the study.
Previous work has shown that external pressures on plants can induce changes such as genomic rearrangement, transposable element activation, and increased homologous recombination. To see if such changes can be passed on to a plant's offspring, researchers led by Jean Molinier, then at Friedrich Miescher Institute for Biomedical Research in Basel, Switzerland, exposed Arabidopsis thaliana plants to one of two stressors: shortwave (UV-C) radiation or flagellin, a protein component of many pathogenic bacteria.
As expected from previous work, the plants treated with radiation or flagellin displayed an increased level of homologous recombination -- a sign of decreased genomic stability that the authors say may allow adaptation to the environment. "It may either be direct adaptive evolution -- plants would be more resistant to UV or to pathogens -- or it could be indirect, by increasing the potential for adaptive evolution," senior author Barbara Hohn, also at Friedrich Miescher Institute, told The Scientist in an Email.
When the researchers allowed the plants to self-pollinate, they found that the treated plants' progeny also displayed increased levels of homologous recombination -- even though they had never been exposed to radiation or flagellin themselves. This effect persisted for at least four generations after the plants were treated.
The researchers also crossed treated males with untreated females and vice versa. They found that the progeny of these crosses showed just as much homologous recombination as when the treated plants were self-pollinated, indicating that the effect can be inherited through both types of gametes in a dominant manner.
The results are "somewhat surprising," said Christopher Cullis of Case Western Reserve University in Cleveland, who was not involved in the study. The idea that "the way that plants grow" can affect their offspring "is still not mainstream," he said.
The mechanism underlying this transgenerational effect is almost certainly epigenetic, Hohn told The Scientist, "because the whole population is affected. If it were mutation...only a tiny, tiny fraction of all plants would have changed to increased recombination behavior."
"You'd have to resequence the genome to be sure," said Virginia Walbot of Stanford University, who was not involved in the study, "but I think overall, the weight of evidence is for an epigenetic [mechanism]."
Exactly what epigenetic mechanism is involved is not clear, though. "They don't know whether it's, for example, some global change in chromatin or some effect on the recombination machinery," Henikoff said. "Maybe there is some change in the chromatin that is allowing the recombination to occur. It might or might not be regulated by DNA methylation.... There are a lot of possibilities here."
Whatever the mechanism, increased genomic flexibility through recombination may enable the genomes of treated plants and their offspring to undergo adaptive evolution, according to the authors.
"Why [genomic flexibility is] a response to a relatively short-term stress is a question that is more difficult to decide," Cullis told The Scientist. "It's a transient stress and yet the plant appears to be making this long-term commitment."
Even so, "adaptive epigenetic changes are probably pretty common in plants," Henikoff said. In animals, epigenetic changes like DNA methylation largely gets erased in germline cells, but "in plants, there's nothing like that," Henikoff said, so plants could more easily pass on acquired epigenetic changes to their progeny.
According to Walbot, the researchers' results are reminiscent of the idea of "genomic challenge" proposed by Barbara McClintock -- that environmental stressors can cause the plant genome to diversify. "In [McClintock's] case it was transposons, but the mechanisms that underlie what the Hohn lab found will be equally interesting," Walbot said.
Melissa Lee Phillips
Links within this article
J. Molinier et al., "Transgeneration memory of stress in plants," Nature, published online August 6, 2006.
C.A. Cullis, "Mechanisms and control of rapid genomic changes in flax," Annals of Botany, January 2005.
J.P. Mottinger et al., "Mutations of the Adh1 gene in maize following infection with barley stripe mosaic virus," Molecular and General Genetics, June 1984.
I. Kovalchuk et al., "Genome-wide variation of the somatic mutation frequency in transgenic plants," The EMBO journal, September 1, 2000.
G. Ries et al., "Elevated UV-B radiation reduces genome stability in plants," Nature, July 6, 2000.
J.B. Weitzman, "Stress-induced recombination," The Scientist, February 19, 2002.
L.A. Pray, "Epigenetics: Genome, meet your environment," The Scientist, July 5, 2004.
Significance of the responses of the genome to challenge, Nobel lecture, December 8, 1983.
"Barbara McClintock, On Her Own," The Scientist, April 21, 2003.