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

PLoS Pathogens

Christopher N. Davis¹  Jack H. Westwood¹  Alison Reed¹  Elizabeth Miller¹  John P. Carr¹  Sophie I. Robinson¹  Sanjie Jiang¹  Simon C. Groen¹  Nik J. Cunniffe¹  Alex M. Murphy¹  Matthew P. Davey¹  Oliver J. Furzer¹  Beverley J. Glover¹  Toby J. A. Bruce²  John C. Caulfield²  John A. Pickett²  Heather M. Whitney³ 

[1]Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom

[2]Rothamsted Research, Harpenden, Hertfordshire, United Kingdom

[3]University of Bristol, School of Biological Sciences, Bristol, United Kingdom

关键词: Flowering plants;    Tomatoes;    Bumblebees;    Flowers;    Bees;    Seeds;    Volatile organic compounds;    Arabidopsis thaliana;   

DOI  :  10.1371/journal.ppat.1005790

学科分类：生物科学（综合）

来源: Public Library of Science

【 摘 要 】

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.

【 授权许可】

CC BY