Virus Infection of Plants Alters Pollinator Preference: A Payback for Susceptible Hosts?

Abstract

Plant volatiles play important roles in attraction of certain pollinators and in host location by herbivorous insects. Virus infection induces changes in plant volatile emission profiles, and this can make plants more attractive to insect herbivores, such as aphids, that act as viral vectors. However, it is unknown if virus-induced alterations in volatile production affect plant-pollinator interactions. We found that volatiles emitted by cucumber mosaic virus (CMV)-infected tomato ( Solanum lycopersicum) and Arabidopsis thaliana plants altered the foraging behaviour of bumblebees ( Bombus terrestris). Virus-induced quantitative and qualitative changes in blends of volatile organic compounds emitted by tomato plants were identified by gas chromatography-coupled mass spectrometry. Experiments with a CMV mutant unable to express the 2b RNA silencing suppressor protein and with Arabidopsis silencing mutants implicate microRNAs in regulating emission of pollinator-perceivable volatiles. In tomato, CMV infection made plants emit volatiles attractive to bumblebees. Bumblebees pollinate tomato by ‘buzzing’ (sonicating) the flowers, which releases pollen and enhances self-fertilization and seed production as well as pollen export. Without buzz-pollination, CMV infection decreased seed yield, but when flowers of mock-inoculated and CMV-infected plants were buzz-pollinated, the increased seed yield for CMV-infected plants was similar to that for mock-inoculated plants. Increased pollinator preference can potentially increase plant reproductive success in two ways: i) as female parents, by increasing the probability that ovules are fertilized; ii) as male parents, by increasing pollen export. Mathematical modeling suggested that over a wide range of conditions in the wild, these increases to the number of offspring of infected susceptible plants resulting from increased pollinator preference could outweigh underlying strong selection pressures favoring pathogen resistance, allowing genes for disease susceptibility to persist in plant populations. We speculate that enhanced pollinator service for infected individuals in wild plant populations might provide mutual benefits to the virus and its susceptible hosts.

Author Summary

Cucumber mosaic virus, an important pathogen of tomato, causes plants to emit volatile chemicals that attract bumblebees. Bumblebees are important tomato pollinators, but do not transmit this virus. We propose that under natural conditions, helping host reproduction by encouraging bee visitation might represent a ‘payback’ by the virus to susceptible hosts. Although tomato flowers can give rise to seed through self-fertilization, bumblebee-mediated ‘buzz-pollination’ enhances this, increasing the number of seeds produced per fruit. Buzz-pollination further favors reproductive success of a plant by facilitating pollen export. Mathematical modeling suggests that if self-fertilization by infected plants, as well as pollen transfer from these plants (cross-fertilization) to surrounding plants is increased, this might favor reproduction of susceptible over that of resistant plants. This raises the possibility that under natural conditions some viruses might enhance competitiveness of susceptible plants and inhibit the emergence of resistant plant strains. We speculate that it may be in a virus’ interest to pay back a susceptible host by enhancing its attractiveness to pollinators, which will likely increase fertilization rates and the dissemination of susceptible plant pollen and may compensate for a decreased yield of seeds on the virus-infected plants.