title: 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.
authors: Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom.
authors: Simon C
authors: SC
authors: Groen
authors: Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom.
authors: Sanjie
authors: S
authors: Jiang
authors: Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom.
authors: Alex M
authors: AM
authors: Murphy
authors: Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom.
authors: Nik J
authors: NJ
authors: Cunniffe
authors: Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom.
authors: Jack H
authors: JH
authors: Westwood
authors: Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom.
authors: Matthew P
authors: MP
authors: Davey
authors: Rothamsted Research, Harpenden, Hertfordshire, United Kingdom.
authors: Toby J A
authors: TJ
authors: Bruce
authors: Rothamsted Research, Harpenden, Hertfordshire, United Kingdom.
authors: John C
authors: JC
authors: Caulfield
authors: Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom.
authors: Oliver J
authors: OJ
authors: Furzer
authors: Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom.
authors: Alison
authors: A
authors: Reed
authors: Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom.
authors: Sophie I
authors: SI
authors: Robinson
authors: Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom.
authors: Elizabeth
authors: E
authors: Miller
authors: Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom.
authors: Christopher N
authors: CN
authors: Davis
authors: Rothamsted Research, Harpenden, Hertfordshire, United Kingdom.
authors: John A
authors: JA
authors: Pickett
authors: University of Bristol, School of Biological Sciences, Bristol, United Kingdom.
authors: Heather M
authors: HM
authors: Whitney
authors: Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom.
authors: Beverley J
authors: BJ
authors: Glover
authors: Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom.
authors: John P
authors: JP
authors: Carr
mesh_terms: D000818:Animals; D017360:Arabidopsis / Q000502:physiology / Q000821:virology*; D001516:Bees / Q000502:physiology*; D017799:Cucumovirus; D005247:Feeding Behavior / Q000502:physiology; D008401:Gas Chromatography-Mass Spectrometry; D018551:Solanum lycopersicum / Q000502:physiology / Q000821:virology*; D008962:Models, Theoretical; D010935:Plant Diseases / Q000821:virology; D054817:Pollination / Q000502:physiology; D055549:Volatile Organic Compounds / Q000378:metabolism
chemical_list: D055549:Volatile Organic Compounds