In the age of industrial agriculture, seeds are often purchased in bulk from corporate growers that use heavy doses of pesticides. They then travel many miles to a farm where climate, soil and pest conditions are dramatically different. As a result, crops often encounter new ailments that never impacted first generation seed plants, which may have been protected from the most troublesome invaders.

This might not be the best approach, based on three studies published in the February issue of Plant Physiology. Not only does adversity in the parent generation appear to make the seed stronger, but it primes plants to fight the specific ailments that plagued their parents.

“We show that exposing tomato plants to some level of caterpillar herbivory will increase resistance for future plants—it’s sort of like a plant vaccine,” says Sergio Rasmann, a biologist at the University of Lausanne in Switzerland.

Rasmann isn’t the only one seeing this effect. In a similar study, Ann Slaughter of the Universite de Neuchatel in Switzerland infected Arabidopsis thaliana plants with a benign strain of the bacteria Pseudomonas syringae (PstavrRpt2). The offspring were more resistant to disease than control groups, which were not infected in the first generation.

How does pest resistance get inherited? Researchers point to epigenetic mechanisms, which regulate gene expression and can be passed from one generation to the next without any changes to DNA sequences. The studies suggest known epigenetic factors like DNA methylation and histone modification mediate these effects, and are among the first to demonstrate siRNAs act as an epigenetic mechanism in plant defense responses.

If similar mechanisms are at work in corn and soy, more resistant seeds might be prepared, ultimately reducing dependencies on pesticides and genetically modified organisms. For example, hormone sprays might induce a defense response in parent plants and prime offspring to respond more quickly. It would likely take far fewer resources to spray a small plot of seed plants than to treat an industrial-size crop field with pesticides. Similarly, using pests and hormones to induce plant responses does not modify the underlying genetic material. “Our findings argue in favor of a natural mechanism that would not require the use of Genetically Modified Organisms for reducing pest populations,” says Rasmann.

Using Pests to Control Pests

Exposing parent plants to a cocktail of local pests might allow farmers to protect plants against site-specific invaders. “Once we have identified the underlying mechanisms, it may be possible to optimize treatments that elicit transgenerational defense priming,” says Jurriaan Ton, a lecturer at the University of Sheffield in the United Kingdom.

Yet plants probably won’t develop disease resistance to all pests, and success may depend on the insect species used to trigger the response. When Rasmann exposed parent plants to the white cabbage butterfly (Pieris rapae), offspring were more resistant to the beet armyworm (Spodoptera exigua) as well. These animals were 40 percent smaller on plants whose parents were exposed. But this doesn’t seem to involve a general defense against all pests; the diamondback moth (Plutella xylostella) was not impacted by the transgenerational resistance.

A slightly different resistance profile was observed when parent plants were exposed to the diamondback moth. Both the white cabbage butterfly and the beet armyworm were less abundant on second generation plants. The cabbage looper (Trichoplusia ni) remained unperturbed by the defense response, as did the diamondback moth, showing that plants don’t develop a memory response to all invading species.

Even more puzzling are findings that show exposure can make plants more susceptible to disease. After Ton and his colleagues exposed Arabidopsis thaliana to the pathogenic bacteria Pseudomonas syringae (PstDC3000), offspring were less resistant to a common fungal disease. The second generation plants became more susceptible to Alternaria brassicicola—the fungus that causes black spot disease in broccoli, cabbage and mustard. The results weren’t entirely grim, however, as plants also showed improved resistance to Pseudomonas and the fungus-like Hyaloperonospora arabidopsidis,

“If we understood the details of the priming mechanisms, it might be possible to breed lines that contain the beneficial but not the detrimental aspects of transgenerational resistance to a particular pest or disease,” says Mike Roberts, a lecturer at Lancaster University in the United Kingdom, who collaborated with Ton on the study.

Roberts and Ton found that exposing plants to bacteria switched the disease response at the molecular level. The genes activated by the plant defense hormone jasmonic acid were less responsive in second generation plants; in contrast, the genes targeted by the hormone salicylic acid were more active. The changes in gene expression correlated with chemical modification of histones—proteins that help control the structure of DNA inside the cell.

Understanding Memory Mechanisms

The findings are among the first to describe next generation plant defense memory, and are laudable for demonstrating the potential mechanisms, says Corné Pieterse, editor of Plant Physiology. Yet when it comes to applications, more research is needed before results can be integrated into agriculture.

“So far the published reports just provide correlations. The findings are still preliminary,” says Uwe Conrath, of RWTH Aachen University in Germany. Conrath has no affiliation with the studies.

The role of siRNAs is the biggest mystery. Rasmann originally turned to small interfering RNAs (siRNAs) while in search of signals that could travel from the site of damage to the embryo. These regulatory molecules are small enough to easily pass from cell to cell. However siRNAs have not yet been shown to pass from one generation to another—an important criteria for an inheritance mechanism.

Rasmann didn’t address this question directly. Instead, he grew two classes of mutant plants that lacked siRNAs—either due to missing nuclear RNA polymerases or defects in the enzymes that dice RNAs into siRNAs. The mutants were generally indistinguishable from the wild type, but showed no transgenerational defenses. While caterpillar infestations triggered chemical defenses in parent generations, the heightened response did not appear in offspring.

The findings are among the first to suggest that siRNAs function as an epigenetic factor in plant memory, although their specific role in the plant defense response must still be demonstrated. “Our sense is that feeding damage from herbivores induces the production of siRNAs that are specific for silencing regions of the [genes] related to the jasmonate pathway,” says Rasmann. “This hypothesis has not been tested, and it is currently under investigation.”

In this sea of unknowns, there is at least one take-home message: epigenetic factors appear to be the vehicle by which plants transfer defense memories to offspring. Further evidence for this comes from the finding that the “grandchildren” of exposed plants inherit the defense memory, but the fourth generation does not. “The observation that inherited resistance reverts after three generations suggests the underlying mechanism is not a mutation or another stable genetic change,” says Georg Jander, a biologist at the Boyce Thompson Institute in Ithaca, NY who partnered with Rasmann.

In this experiment parent plants were exposed to caterpillars, but second generation plants were kept protected from the pests. The third generation’s heightened response to caterpillar invasions was thus presumably due to the first generation’s exposure. But plant defenses reverted back to normal in later generations, indicating epigenetics were probably at work.

Agricultural Applications

Despite the uncertainties, the findings potentially have broad applications to many different types of crops. While techniques are aren’t yet marketable, Conrath says large agricultural companies are already beginning to take interest. Last year he published one of the only previous reports on transgenerational plant memory responses in the journal EMBO reports. “Since then I have been invited to present to various big-player companies working in plant protection,” he says. “It’s becoming increasingly clear that the phenomenon is relevant to applied plant protection.”

The strategy may be particularly useful for small-scale farmers in developing countries. “If farmers learn to collect seeds from defense-expressing plants without transmitting plant disease through the seed, it would be relatively cost-efficient to obtain crops that are better adapted to cope with local disease pressures,” says Ton, although he warns there is no silver bullet.

Without the ability to amplify epigenetic signals—either by tailoring pest exposure or with hormonal applications—the disease response will only rarely reach the levels of protection commonly obtained by pesticides. “The resulting levels of disease and pest resistance remain relatively weak,” says Ton. “I nevertheless believe there is a very strong potential for exploitation of the phenomenon, particularly in integrated pest management strategies that minimize pesticide exposure and intensify sustainable crop production.”

In regions like the corn and soy belt of America’s Midwest, where chemical pollution has reached high levels, even moderate reductions in herbicide and pesticide use could have ecological and public health benefits. This is why researchers will now begin testing their methods on domestic crop cultivars. Ton is preparing experiments on tomato plants, while Jander and Roberts will soon begin research on Maize. If all goes well, seed farms may one day intentionally infest plants with insects and bacteria.

Plant physiology, 2012. DOI: 10.1104/pp.111.187831, 10.1104/pp.111.187468 , 10.1104/pp.111.191593 (About DOIs).