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.
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Claims 8
Claim · model-written summary
Volatiles from CMV-infected tomato altered bumblebee foraging.
- Taxon
- tomato
Solanum lycopersicume0 - Interactor
- bumblebees (Bombus terrestris)
Bombus terrestrise0pollinator - Second interactor
- cucumber mosaic virus (CMV)
cucumber mosaic cucumoviruse0pathogen
- Outcome
- foraging behaviour of bumblebeese0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.


Verbatim
e0“volatiles emitted by cucumber mosaic virus (CMV)-infected tomato (Solanum lycopersicum) and Arabidopsis thaliana plants altered the foraging behaviour of bumblebees (Bombus terrestris).”
Claim · model-written summary
Volatiles from CMV-infected Arabidopsis altered bumblebee foraging.
- Taxon
- Arabidopsis thaliana
Arabidopsis thalianae0 - Interactor
- bumblebees (Bombus terrestris)
Bombus terrestrise0pollinator - Second interactor
- cucumber mosaic virus (CMV)
cucumber mosaic cucumoviruse0pathogen
- Outcome
- foraging behaviour of bumblebeese0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.


Verbatim
e0“volatiles emitted by cucumber mosaic virus (CMV)-infected tomato (Solanum lycopersicum) and Arabidopsis thaliana plants altered the foraging behaviour of bumblebees (Bombus terrestris).”
Claim · model-written summary
CMV infection changed the quantity and composition of tomato volatile blends.
- Taxon
- tomato
Solanum lycopersicume0 - Interactor
- Viruse0pathogen
- Outcome
- quantitative and qualitative changes in blends of volatile organic compoundse0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Verbatim
e0“Virus-induced quantitative and qualitative changes in blends of volatile organic compounds emitted by tomato plants were identified by gas chromatography-coupled mass spectrometry.”
Claim · model-written summary
CMV 2b and Arabidopsis silencing mutant experiments implicated microRNAs in pollinator-perceivable volatile emission.
- Taxon
- Arabidopsis
Arabidopsise0 - Interactor
- CMV
cucumber mosaic cucumoviruse0pathogen
- Gene
- microRNAse0
- Outcome
- emission of pollinator-perceivable volatilese0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Verbatim
e0“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.”
Claim · model-written summary
CMV infection made tomato volatiles attractive to bumblebees.
- Taxon
- tomato
Solanum lycopersicume0 - Treatment
- CMV infectione0
- Interactor
- CMV
cucumber mosaic cucumoviruse0pathogen
- Outcome
- volatiles attractive to bumblebeese0
Not reportedComparatorDirection
Organisms pictured · Representative pictures of the matched species, not figures from the paper.


Verbatim
e0“In tomato, CMV infection made plants emit volatiles attractive to bumblebees.”
Claim · model-written summary
Without buzz pollination, CMV infection reduced tomato seed yield.
- Taxon
- tomato
Solanum lycopersicume1 - Treatment
- CMV infectione0
- Interactor
- CMV
cucumber mosaic cucumoviruse0pathogen
- Outcome
- seed yielde0
- Direction
- decreasede0
- Qualifier
- Without buzz-pollinatione0
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Verbatim
e0“Without buzz-pollination, CMV infection decreased seed yield”
e1“In tomato, CMV infection made plants emit volatiles attractive to bumblebees.”
Claim · model-written summary
With buzz pollination, CMV-infected tomato seed yield increased similarly to mock-inoculated plants.
- Taxon
- tomato
Solanum lycopersicume1 - Treatment
- buzz-pollinatede0
- Interactor
- CMV
cucumber mosaic cucumoviruse0pathogen
- Outcome
- seed yielde0
- Direction
- increasede0
- Comparator
- mock-inoculatede0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Verbatim
e0“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.”
e1“In tomato, CMV infection made plants emit volatiles attractive to bumblebees.”
Claim · model-written summary
Modeling suggested pollinator preference could offset selection for resistance and allow susceptibility genes to persist.
- Taxon
- plantsViridiplantaee0
- Outcome
- genes for disease susceptibility to persist in plant populationse0
- Qualifier
- over a wide range of conditions in the wilde0
Verbatim
e0“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.”
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