A bout of a viral infection can leave tomato plants stunted and their leaves sickly. But it might offer a surprising reproductive boost: infected plants release a different smell than healthy ones, and that unique aroma can draw more bees in to pollinate flowers and make more seeds. The results, published August 11 in PLOS Pathogens, suggest that this increase in pollination may offer benefits to both the pathogen and its host plants.
The virus in question, known as cucumber mosaic virus (CMV) infects more than 1200 different plant species. “Many of us have focused on what makes this virus such a successful pathogen,” says molecular virologist Shou-wei Ding of the University of California, Riverside, who was not involved in the research. “This study reveals the plant’s side of the story: it suggests that one reason could be that the plant community welcomes the virus because of this potentially beneficial effect.”
Previous studies have found that CMV makes a protein known as 2b, which alters volatile chemicals made by plants to make them more attractive to aphids, the sapsucking insects that spread the virus. But John Carr of the University of Cambridge and his colleagues wanted to test if the virus could also affect the behavior of pollinators such as bees.
Bees were allowed to fly freely through a greenhouse containing healthy plants, CMV-infected ones, and plants infected with CMVΔ2b, a mutated form of the virus that lacked the 2b protein. Although the plants were covered with towers so insects couldn’t see differences—only smell them—the bees were more attracted to virus-infected plants than uninfected ones. But mutated forms of the virus failed to create this buzz.
“We were very surprised to find that not only did the bumblebees like one group of plants over the other, but they also liked the smell of sick plants,” says Carr. “It didn’t make sense because the bees don’t transmit this particular virus.”
So why were the insects attracted by a whiff of an infection? When insects were allowed to see and sniff flowers, the team found bees were still more attracted to CMV-infected plants—and spent a greater amount of time pollinating them. Diseased plants make fewer seeds and fruit in the absence of bees. But when the pollinators were present, virus-carrying plants made 6-7 times more seeds than when bees were absent.
Carr suggests that this may be a form of payback: by helping infected plants attract bees and make more seeds, the virus creates an advantage for plants that are susceptible to infection. Using a mathematical simulation to assess the long-term impact of this viral effect, the researchers suggest that the increase in seed production could potentially explain why plants in the wild may have failed to evolve resistance to the virus.
The CMV2b protein is known to suppress silencers such as the Argonaute 1 protein, which regulates microRNA and short interfering RNA-mediated signaling pathways. These signaling pathways control plants’ production of volatile chemicals. Testing the smells produced by infected and healthy tomato plants, Carr and his colleagues found distinct differences in the odorant chemicals released by healthy and infected plants.
But precisely how the virus exerts its effects via miRNA signaling pathways isn’t clear. “What host pathways and molecular mechanisms control this virus-induced attraction to the bumblebees still needs to be investigated,” says Ding.