Paper · 2016 · PLoS Pathogens

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

Simon C. Groen; Sanjie Jiang; Alex M. Murphy; et al.

8
claims
10
verbatim quotes
101
citations
6
research areas
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Open access · cc-by

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.

Abstract from the paper’s OpenAlex record; open copy licensed cc-by. Read at the source ↗

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Claims 8

Observationobservedoriginal resultmeasured

Claim · model-written summary

Volatiles from CMV-infected tomato altered bumblebee foraging.

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.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗
Bombus terrestris
Bombus terrestris · InteractorIvar Leidus · CC BY-SA 4.0 · Wikimedia Commons ↗
cucumber mosaic cucumovirus
cucumber mosaic cucumovirus · Second interactorDieterO · Public domain · Wikimedia Commons ↗

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).”

✓ located verbatim in the source · abstract, characters 421–606 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Volatiles from CMV-infected Arabidopsis altered bumblebee foraging.

Taxon
Arabidopsis thalianaArabidopsis 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.

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗
Bombus terrestris
Bombus terrestris · InteractorIvar Leidus · CC BY-SA 4.0 · Wikimedia Commons ↗
cucumber mosaic cucumovirus
cucumber mosaic cucumovirus · Second interactorDieterO · Public domain · Wikimedia Commons ↗

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).”

✓ located verbatim in the source · abstract, characters 421–606 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

CMV infection changed the quantity and composition of tomato volatile blends.

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.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

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.”

✓ located verbatim in the source · abstract, characters 607–787 · show in text ↑
Mechanismobservedoriginal resultmeasured

Claim · model-written summary

CMV 2b and Arabidopsis silencing mutant experiments implicated microRNAs in pollinator-perceivable volatile emission.

Taxon
ArabidopsisArabidopsise0
Interactor
CMVcucumber mosaic cucumoviruse0pathogen
Gene
microRNAse0
Outcome
emission of pollinator-perceivable volatilese0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Arabidopsis
Arabidopsis · Taxon · picture of the genus (one of its species)Original uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗
cucumber mosaic cucumovirus
cucumber mosaic cucumovirus · InteractorDieterO · Public domain · Wikimedia Commons ↗

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.”

✓ located verbatim in the source · abstract, characters 788–994 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

CMV infection made tomato volatiles attractive to bumblebees.

Treatment
CMV infectione0
Interactor
CMVcucumber mosaic cucumoviruse0pathogen
Second interactor
bumblebeesBombuse0pollinator
Outcome
volatiles attractive to bumblebeese0

Not reportedComparatorDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗
cucumber mosaic cucumovirus
cucumber mosaic cucumovirus · InteractorDieterO · Public domain · Wikimedia Commons ↗
Bombus
Bombus · Second interactor · picture of the genus (one of its species)Marco Almbauer · CC0 · Wikimedia Commons ↗

Verbatim

e0

“In tomato, CMV infection made plants emit volatiles attractive to bumblebees.”

✓ located verbatim in the source · abstract, characters 995–1072 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Without buzz pollination, CMV infection reduced tomato seed yield.

Treatment
CMV infectione0
Interactor
CMVcucumber 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.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗
cucumber mosaic cucumovirus
cucumber mosaic cucumovirus · InteractorDieterO · Public domain · Wikimedia Commons ↗

Verbatim

e0

“Without buzz-pollination, CMV infection decreased seed yield”

✓ located verbatim in the source · abstract, characters 1240–1300 · show in text ↑
e1

“In tomato, CMV infection made plants emit volatiles attractive to bumblebees.”

✓ located verbatim in the source · abstract, characters 995–1072 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

With buzz pollination, CMV-infected tomato seed yield increased similarly to mock-inoculated plants.

Treatment
buzz-pollinatede0
Interactor
CMVcucumber mosaic cucumoviruse0pathogen
Outcome
seed yielde0
Direction
increasede0
Comparator
mock-inoculatede0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗
cucumber mosaic cucumovirus
cucumber mosaic cucumovirus · InteractorDieterO · Public domain · Wikimedia Commons ↗

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.”

✓ located verbatim in the source · abstract, characters 1306–1480 · show in text ↑
e1

“In tomato, CMV infection made plants emit volatiles attractive to bumblebees.”

✓ located verbatim in the source · abstract, characters 995–1072 · show in text ↑
Observationauthor interpretationoriginal resultmixedsimulated

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.”

✓ located verbatim in the source · abstract, characters 1708–2068 · show in text ↑

Cucumis sativus · cucumber mosaic cucumovirus · Solanum lycopersicum (tomato)Positive and negative results

22 papers: 10 positive, 12 negative or no effect

9 papers in the same direction as this paper · 12 in the opposite direction

  1. negative
  2. negative
  3. negative

18 papers more in this group

See all 22 papers →

infection · cucumber mosaic cucumovirus · Solanum lycopersicum (tomato)Positive and negative results

7 papers: 1 positive, 6 negative or no effect

6 in the opposite direction

  1. negative
  2. negative
  3. negative

3 papers more in this group

See all 7 papers →

Claims are grouped by organism, treatment and what was measured or targeted. A paper counts as positive when any of its claims in the group is positive.