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

Groen, SC; Jiang, S; Murphy, AM; Cunniffe, NJ; Westwood, JH; Davey, MP; Bruce, T; Caulfield, JC; Furzer, OJ; Reed, A; Robinson, SI; Miller, E; Davis, CN; Pickett, JA; Whitney, HM; Glover, BJ; Carr, JP

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Authors

SC Groen

S Jiang

AM Murphy

NJ Cunniffe

JH Westwood

MP Davey

JC Caulfield

OJ Furzer

A Reed

SI Robinson

E Miller

CN Davis

JA Pickett

HM Whitney

BJ Glover

JP Carr



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.

Acceptance Date Jul 6, 2016
Publication Date Aug 11, 2016
Publicly Available Date Mar 28, 2024
Journal PLoS Pathogens
Print ISSN 1553-7374
Publisher Public Library of Science
Pages e1005790 - ?
DOI https://doi.org/10.1371/journal.ppat.1005790
Keywords virus, infection, plants, pollinator, susceptible.
Publisher URL https://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1005790

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