Cargando…
Virus Infection of Plants Alters Pollinator Preference: A Payback for Susceptible Hosts?
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. Howeve...
Autores principales: | , , , , , , , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2016
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4981420/ https://www.ncbi.nlm.nih.gov/pubmed/27513727 http://dx.doi.org/10.1371/journal.ppat.1005790 |
_version_ | 1782447612439298048 |
---|---|
author | Groen, Simon C. Jiang, Sanjie Murphy, Alex M. Cunniffe, Nik J. Westwood, Jack H. Davey, Matthew P. Bruce, Toby J. A. Caulfield, John C. Furzer, Oliver J. Reed, Alison Robinson, Sophie I. Miller, Elizabeth Davis, Christopher N. Pickett, John A. Whitney, Heather M. Glover, Beverley J. Carr, John P. |
author_facet | Groen, Simon C. Jiang, Sanjie Murphy, Alex M. Cunniffe, Nik J. Westwood, Jack H. Davey, Matthew P. Bruce, Toby J. A. Caulfield, John C. Furzer, Oliver J. Reed, Alison Robinson, Sophie I. Miller, Elizabeth Davis, Christopher N. Pickett, John A. Whitney, Heather M. Glover, Beverley J. Carr, John P. |
author_sort | Groen, Simon C. |
collection | PubMed |
description | 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. |
format | Online Article Text |
id | pubmed-4981420 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2016 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-49814202016-08-29 Virus Infection of Plants Alters Pollinator Preference: A Payback for Susceptible Hosts? Groen, Simon C. Jiang, Sanjie Murphy, Alex M. Cunniffe, Nik J. Westwood, Jack H. Davey, Matthew P. Bruce, Toby J. A. Caulfield, John C. Furzer, Oliver J. Reed, Alison Robinson, Sophie I. Miller, Elizabeth Davis, Christopher N. Pickett, John A. Whitney, Heather M. Glover, Beverley J. Carr, John P. PLoS Pathog Research Article 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. Public Library of Science 2016-08-11 /pmc/articles/PMC4981420/ /pubmed/27513727 http://dx.doi.org/10.1371/journal.ppat.1005790 Text en © 2016 Groen et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited. |
spellingShingle | Research Article Groen, Simon C. Jiang, Sanjie Murphy, Alex M. Cunniffe, Nik J. Westwood, Jack H. Davey, Matthew P. Bruce, Toby J. A. Caulfield, John C. Furzer, Oliver J. Reed, Alison Robinson, Sophie I. Miller, Elizabeth Davis, Christopher N. Pickett, John A. Whitney, Heather M. Glover, Beverley J. Carr, John P. Virus Infection of Plants Alters Pollinator Preference: A Payback for Susceptible Hosts? |
title | Virus Infection of Plants Alters Pollinator Preference: A Payback for Susceptible Hosts? |
title_full | Virus Infection of Plants Alters Pollinator Preference: A Payback for Susceptible Hosts? |
title_fullStr | Virus Infection of Plants Alters Pollinator Preference: A Payback for Susceptible Hosts? |
title_full_unstemmed | Virus Infection of Plants Alters Pollinator Preference: A Payback for Susceptible Hosts? |
title_short | Virus Infection of Plants Alters Pollinator Preference: A Payback for Susceptible Hosts? |
title_sort | virus infection of plants alters pollinator preference: a payback for susceptible hosts? |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4981420/ https://www.ncbi.nlm.nih.gov/pubmed/27513727 http://dx.doi.org/10.1371/journal.ppat.1005790 |
work_keys_str_mv | AT groensimonc virusinfectionofplantsalterspollinatorpreferenceapaybackforsusceptiblehosts AT jiangsanjie virusinfectionofplantsalterspollinatorpreferenceapaybackforsusceptiblehosts AT murphyalexm virusinfectionofplantsalterspollinatorpreferenceapaybackforsusceptiblehosts AT cunniffenikj virusinfectionofplantsalterspollinatorpreferenceapaybackforsusceptiblehosts AT westwoodjackh virusinfectionofplantsalterspollinatorpreferenceapaybackforsusceptiblehosts AT daveymatthewp virusinfectionofplantsalterspollinatorpreferenceapaybackforsusceptiblehosts AT brucetobyja virusinfectionofplantsalterspollinatorpreferenceapaybackforsusceptiblehosts AT caulfieldjohnc virusinfectionofplantsalterspollinatorpreferenceapaybackforsusceptiblehosts AT furzeroliverj virusinfectionofplantsalterspollinatorpreferenceapaybackforsusceptiblehosts AT reedalison virusinfectionofplantsalterspollinatorpreferenceapaybackforsusceptiblehosts AT robinsonsophiei virusinfectionofplantsalterspollinatorpreferenceapaybackforsusceptiblehosts AT millerelizabeth virusinfectionofplantsalterspollinatorpreferenceapaybackforsusceptiblehosts AT davischristophern virusinfectionofplantsalterspollinatorpreferenceapaybackforsusceptiblehosts AT pickettjohna virusinfectionofplantsalterspollinatorpreferenceapaybackforsusceptiblehosts AT whitneyheatherm virusinfectionofplantsalterspollinatorpreferenceapaybackforsusceptiblehosts AT gloverbeverleyj virusinfectionofplantsalterspollinatorpreferenceapaybackforsusceptiblehosts AT carrjohnp virusinfectionofplantsalterspollinatorpreferenceapaybackforsusceptiblehosts |