Published online 6 August 2006 | Nature | doi:10.1038/news060731-16

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Increased tendency to mutate is handed down to next generation.

A parent plant can pass the tendency to mutate on to its offspring. © SPL

Plants under stress not only activate their own defences, but also manage to pass on a possible protective strategy to their descendants. That's the surprising conclusion of a study published online today by Nature1.

Stresses such as pathogen infection or ultraviolet radiation can trigger increased rates of genetic mutation in some plant cells, occasionally even scrambling regions of their DNA. Some scientists hypothesize that by augmenting their genomic flexibility, plants boost their ability to produce genetic changes that could allow them to adapt to stressful environments. Now it seems that plants can also pass this genetic pliability on to their offspring.

Researchers in Barbara Hohn's lab at the Friedrich Miescher Institute for Biomedical Research in Basel, Switzerland, study a process in which one piece of DNA within the genome replaces another fragment of similar sequence. This process, called 'homologous recombination', occurs more frequently in stressed plants. Plants grown near the site of the Chernobyl nuclear-reactor accident, for example, were found to have rates of homologous recombination that increased with the dose of radiation they received.

By chance, a student in Hohn's lab found that the rate of homologous recombination was curiously high in a particular batch of cress plant or Arabidopsis seeds. When he traced back the origin of the seeds, he discovered that the parent had been irradiated.

"Nobody set out to do this," says Hohn. "It was pure serendipity."

Stressful memories

“Nobody set out to do this. It was pure serendipity.” Barbara Hohn

Friedrich Miescher Institute for Biomedical Research.

After the accidental discovery, Hohn's group set out to examine what was going on. The team found that, as expected, giving a parental plant a burst of ultraviolet radiation or a simulated pathogen attack boosted the rate of homologous recombination in some of its cells. And when the change occurred in cells that are used to form the plants' offspring, all progeny carried the genetic change.

But, surprisingly, even if the cells used to create the progeny didn't carry the genetic change, the offspring of the stressed plants were still more likely to undergo homologous recombination in their own cells. They had inherited a tendency to mutate.

The memory of the initial stress lasted a long time; at least four generations had an increased level of homologous recombination.

Exactly how plants pass down this information is unknown. Hohn believes that the mechanism is 'epigenetic' — inheritance of a trait without a corresponding change in DNA sequence. Chemical modification of a plant's DNA that happens during its lifetime, for example, can be copied into the progeny's DNA. Or RNA, an intermediate that helps to convert DNA information into proteins, may be ferried from a parent's cells into its offspring's.

Hohn is quick to point out that her lab has not shown that the progeny of stressed parents are themselves more stress-tolerant, so it is unclear what advantage, if any, this inheritance gives the subsequent generations. "If the plants become UV-resistant or pathogen-resistant," she says, "that would be adaptive evolution." Hohn's lab hasn't yet tested whether this is so.

Staying put

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It makes sense that plants would have elaborate strategies for coping with stress, says Christopher Cullis, a biologist at Case Western Reserve University in Cleveland, Ohio. "Plants can't get up and find somewhere nicer," says Cullis. "So they've got to find a way of coping with that stress." But he finds it surprising that a single burst of stress seems sufficient to trigger such a long-lasting response.

Eric Richards, a biology professor at Washington University in St Louis, says that results from Hohn's lab are intriguing. One interesting follow-up, he adds, is to check whether recombination has increased throughout the plant's entire genome. Hohn's lab is set up to look at just one specific gene, so they haven't yet taken this broader approach.

"I think there's probably a lot more of these inherited epigenetic phenomena out there than people think," says Richards, who himself studies plant epigenetics. "I guess it's now come to the point at which people are starting to take these things seriously."

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Friedrich Miescher Institute for Biomedical Research.