Volatile organic compounds that are emitted by plants – which play important roles in attracting insects – can be altered by virus infection. Infection by cucumber mosaic virus (CMV) increases the emissions that attract aphids, but the virus-altered plant juices are not so tasty, so the insect quickly leaves to spread virus to other plants (listen to TWiV #70 for a full discussion of this finding). Plant pollinators can also respond to plant virus-induced volatile compounds (paper link)
Cucumber mosaic virus is a (+) strand RNA virus that is a pathogen of tomato plants. The virus is spread by aphids, and bumblebees increase fruit yield by buzz-pollination (tomato plants are self-pollinating but bumblebees cause increased seed production).
To study the attraction of bumblebees to tomato plants, the authors encased single tomato plants in a tower topped with a screen and a small cup of 30% sucrose (shown in photo: credit). This arrangement allowed volatile compounds to waft through the screen above the plant.
Bumblebees clearly preferred to visit the CMV-infected over the uninfected plants. They also shunned plants infected with a mutant of CMV that cannot antagonize the RNA interference system of the plant – a major defense against viruses. The results suggest that CMV somehow alters plant produced volatile compounds to attract bumblebee pollinators, and that production of these compounds is regulated by microRNAs.
These findings – that CMV infected plants attract bees via the production of volatiles under the control of microRNAs – were confirmed using Arabidopsis, a model plant which can be genetically manipulated.
Chemical analysis of the volatiles produced by infected and uninfected tomato plants revealed that virus infection reduced the levels of two terpenoids, 2-carene and beta-phellandrene. These compounds are known to repel bumblebees, leading to the suggestion that their reduction may explain why bees prefer infected plants.
Is attraction of bumblebees by viral infection random, or does it have a purpose? CMV infection of tomato plants decreases seed production, an effect that is reversed when bumblebees are attracted to the plants and pollinate them.
The results show that CMV infection of tomato plants causes the emission of volatile compounds that attract pollinating bumblebees, which negate the inhibition of seed production by infection.
Bumblebees do not transmit CMV, so how did this non-fatal attraction come about? One can imagine that at one time CMV infection of plants did not attract bumblebees, and that infection severely depressed plant production. Then a random viral mutant arose that could induce the proper volatiles to attract bumblebees. This change provided a selective advantage because plant seed production was restored by bumblebee pollination. This is called a ‘payback’ hypothesis: the virus has a place to replicate, and the plant lives on due to virus-induced volatile compounds.
I have a bit of trouble with this payback idea, because at the base of it are human-like intentions. Why do we assume that what drives evolution are forces that make sense to us? The plant-centric view is that it was not a CMV mutant, but a plant mutant that arose, which could make the proper bumblebee attractants upon CMV infection. The selective force to maintain such a plant is very clear and involves no anthropocentric ‘payback’.
Whatever the origin of this non-fatal attraction, it merits further study, not only for developing better pollination methods, but for understanding the viral-host symbiosis.