A researcher stands inside the
A researcher stands inside the “flight arena” in the glasshouse of the Cambridge University Botanic Garden. [John Carr/Alex Murphy]

If the ultimate goal of a parasite is to leech off its host enough nutrients to survive without completely destroying the host so it can continue to propagate, then the cucumber mosaic virus (CMV) has become a true master at the art of adaption in the evolutionary struggle for existence. Now, scientists at the University of Cambridge found that CMV alters gene expression in the tomato plants it infects, causing changes to volatile airborne chemicals—the scent—emitted by the plants.

Most interestingly, the researchers found that bees could smell these subtle changes, as glasshouse experiments have shown that bumblebees prefer the infected plants over healthy ones. The Cambridge team believes that by indirectly manipulating bee behavior to improve pollination of infected plants by changing their scent, the virus is effectively paying its host back. Yet, this is not an altruistic mechanism, because it seemingly aids the spread of the pollen to susceptible plants, inhibiting the chance of virus-resistant plant strains emerging.  

The authors of this new study, which was published recently in PLOS Pathogens in an article entitled “Virus Infection of Plants Alters Pollinator Preference: A Payback for Susceptible Hosts?” say that understanding the smells that attract bees, and reproducing these artificially by using similar chemical blends, may enable growers to protect or even enhance yields of bee-pollinated crops.

“Bees provide a vital pollination service in the production of three-quarters of the world's food crops. With their numbers in rapid decline, scientists have been searching for ways to harness pollinator power to boost agricultural yields,” explained senior study author John Carr, Ph.D., head of Cambridge's virology and molecular plant pathology group. “Better understanding the natural chemicals that attract bees could provide ways of enhancing pollination and attracting bees to good sources of pollen and nectar—which they need for survival.”

CMV, typically transmitted by aphids and not by bees, is one of the most prevalent pathogens affecting tomato plants, resulting in small plants with poor-tasting fruits that can cause serious losses to cultivated crops. Not only is CMV one of the most damaging viruses for horticultural crops, but it also persists in wild plant populations, and the authors say their results suggest why.

“We were surprised that bees liked the smell of the plants infected with the virus—it made no sense,” remarked Dr. Carr. “You'd think the pollinators would prefer a healthy plant. However, modeling suggested that if pollinators were biased toward diseased plants in the wild, this could short-circuit natural selection for disease resistance.”

“The virus is rewarding disease-susceptible plants,” he added, “and at the same time producing new hosts it can infect to prevent itself from going extinct. An example, perhaps, of what's known as symbiotic mutualism.”

The investigators describe findings that reveal a new level of complexity in the evolutionary “arms race” between plants and viruses, in which it is traditionally believed that plants continually evolve new forms of disease-resistance while viruses evolve new ways to evade it.

“We would expect the plants susceptible to disease to suffer, but in making them more attractive to pollinators the virus gives these plants an advantage,” noted Dr. Carr. “Our results suggest that the picture of a plant-pathogen arms race is more complex than previously thought, and in some cases, we should think of viruses in a more positive way.”

The blend of volatile organic compounds that plants emit has evolved to perform multiple functions, attracting pollinators and repulsing plant-eating animals and microbes. In the current study, the Cambridge team grew plants in individual containers and collected air with emissions from CMV-infected plants, as well as mock-infected control plants. Using mass spectrometry, the researchers could see the change in emissions induced by the virus. More importantly, they found that bumblebees could smell the changes.

“Bees are far more sensitive to the blends of volatiles emitted by plants and can detect very subtle differences in the mix of chemicals,” Dr. Carr stated. “In fact, they can even be trained to detect traces of chemicals emitted by synthetic substances, including explosives and drugs.”

Finally, the researchers used mathematical modeling to show how pollinator bias for infected plants can cause genes for disease susceptibility to persist in plant populations over vast numbers of generations. With the global population estimated to reach nine billion people by 2050, producing enough food will be one of this century's greatest challenges. The researchers hope that their work will help address issues surrounding food security at local, national, and international scales.








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