Paper · 2016 · mBio

Degradation of the Plant Defense Signal Salicylic Acid Protects Ralstonia solanacearum from Toxicity and Enhances Virulence on Tobacco

Tiffany M. Lowe-Power; Jonathan M. Jacobs; Florent Ailloud; et al.

6
claims
10
verbatim quotes
100
citations
2
research areas
✓
Open access · cc-by

Abstract

UNLABELLED: Plants use the signaling molecule salicylic acid (SA) to trigger defenses against diverse pathogens, including the bacterial wilt pathogen Ralstonia solanacearum SA can also inhibit microbial growth. Most sequenced strains of the heterogeneous R. solanacearum species complex can degrade SA via gentisic acid to pyruvate and fumarate. R. solanacearum strain GMI1000 expresses this SA degradation pathway during tomato pathogenesis. Transcriptional analysis revealed that subinhibitory SA levels induced expression of the SA degradation pathway, toxin efflux pumps, and some general stress responses. Interestingly, SA treatment repressed expression of virulence factors, including the type III secretion system, suggesting that this pathogen may suppress virulence functions when stressed. A GMI1000 mutant lacking SA degradation activity was much more susceptible to SA toxicity but retained the wild-type colonization ability and virulence on tomato. This may be because SA is less important than gentisic acid in tomato defense signaling. However, another host, tobacco, responds strongly to SA. To test the hypothesis that SA degradation contributes to virulence on tobacco, we measured the effect of adding this pathway to the tobacco-pathogenic R. solanacearum strain K60, which lacks SA degradation genes. Ectopic addition of the GMI1000 SA degradation locus, including adjacent genes encoding two porins and a LysR-type transcriptional regulator, significantly increased the virulence of strain K60 on tobacco. Together, these results suggest that R. solanacearum degrades plant SA to protect itself from inhibitory levels of this compound and also to enhance its virulence on plant hosts like tobacco that use SA as a defense signal molecule. IMPORTANCE: Plant pathogens such as the bacterial wilt agent Ralstonia solanacearum threaten food and economic security by causing significant losses for small- and large-scale growers of tomato, tobacco, banana, potato, and ornamentals. Like most plants, these crop hosts use salicylic acid (SA) both indirectly as a signal to activate defenses and directly as an antimicrobial chemical. We found that SA inhibits growth of R. solanacearum and induces a general stress response that includes repression of multiple bacterial wilt virulence factors. The ability to degrade SA reduces the pathogen's sensitivity to SA toxicity and increases its virulence on tobacco.

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Claims 6

Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Subinhibitory SA levels induced expression of the SA degradation pathway, toxin efflux pumps and some general stress responses in R. solanacearum.

Treatment
subinhibitory SA levelse1
Interactor
R. solanacearumRalstonia solanacearume0pathogen
Outcome
expression of the SA degradation pathway, toxin efflux pumps, and some general stress responsese1
Direction
inducede1

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 ↗
Ralstonia solanacearum
Ralstonia solanacearum · InteractorClemson University - USDA Cooperative Extension Slide Series, Bugwood.org · Public domain · Wikimedia Commons ↗

Verbatim

e0

“R. solanacearum strain GMI1000 expresses this SA degradation pathway during tomato pathogenesis”

✓ located verbatim in the source · abstract, characters 347–442 · show in text ↑
e1

“Transcriptional analysis revealed that subinhibitory SA levels induced expression of the SA degradation pathway, toxin efflux pumps, and some general stress responses”

✓ located verbatim in the source · abstract, characters 444–610 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

SA treatment repressed expression of virulence factors, including the type III secretion system, in R. solanacearum.

Treatment
SA treatmente2
Outcome
expression of virulence factorse2
Direction
repressede2

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 ↗

Verbatim

e0

“R. solanacearum strain GMI1000 expresses this SA degradation pathway during tomato pathogenesis”

✓ located verbatim in the source · abstract, characters 347–442 · show in text ↑
e2

“Interestingly, SA treatment repressed expression of virulence factors, including the type III secretion system”

✓ located verbatim in the source · abstract, characters 612–722 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

A GMI1000 mutant lacking SA degradation activity was much more susceptible to SA toxicity.

Treatment
SAe3
Outcome
susceptible to SA toxicitye3
Direction
much more susceptiblee3

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 ↗

Verbatim

e3

“A GMI1000 mutant lacking SA degradation activity was much more susceptible to SA toxicity but retained the wild-type colonization ability and virulence on tomato”

✓ located verbatim in the source · abstract, characters 802–963 · show in text ↑
Observationobservedoriginal resultno effectmeasured

Claim · model-written summary

The GMI1000 mutant lacking SA degradation activity retained wild-type colonization ability and virulence on tomato.

Outcome
colonization ability and virulencee3
Comparator
wild-typee3

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

e3

“A GMI1000 mutant lacking SA degradation activity was much more susceptible to SA toxicity but retained the wild-type colonization ability and virulence on tomato”

✓ located verbatim in the source · abstract, characters 802–963 · show in text ↑
Intervention effectobservedoriginal resultnegativesignificant (as stated)measured

Claim · model-written summary

Adding the GMI1000 SA degradation locus significantly increased the virulence of R. solanacearum strain K60 on tobacco.

Treatment
Ectopic addition of the GMI1000 SA degradation locuse4
Interactor
R. solanacearumRalstonia solanacearume5pathogen
Outcome
virulencee4
Direction
significantly increasede4
Comparator
strain K60e4

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

Nicotiana tabacum
Nicotiana tabacum · TaxonJom / Joachim Müllerchen · CC BY 2.5 · Wikimedia Commons ↗
Ralstonia solanacearum
Ralstonia solanacearum · InteractorClemson University - USDA Cooperative Extension Slide Series, Bugwood.org · Public domain · Wikimedia Commons ↗

Verbatim

e4

“Ectopic addition of the GMI1000 SA degradation locus, including adjacent genes encoding two porins and a LysR-type transcriptional regulator, significantly increased the virulence of strain K60 on tobacco”

✓ located verbatim in the source · abstract, characters 1325–1529 · show in text ↑
e5

“we measured the effect of adding this pathway to the tobacco-pathogenic R. solanacearum strain K60”

✓ located verbatim in the source · abstract, characters 1191–1289 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

SA inhibits growth of R. solanacearum on tomato and induces a general stress response that represses bacterial wilt virulence factors.

Treatment
SAe6
Interactor
R. solanacearumRalstonia solanacearume6pathogen
Outcome
growth of R. solanacearume6
Direction
inhibitse6

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 ↗
Ralstonia solanacearum
Ralstonia solanacearum · InteractorClemson University - USDA Cooperative Extension Slide Series, Bugwood.org · Public domain · Wikimedia Commons ↗

Verbatim

e0

“R. solanacearum strain GMI1000 expresses this SA degradation pathway during tomato pathogenesis”

✓ located verbatim in the source · abstract, characters 347–442 · show in text ↑
e6

“We found that SA inhibits growth of R. solanacearum and induces a general stress response that includes repression of multiple bacterial wilt virulence factors”

✓ located verbatim in the source · abstract, characters 2153–2312 · show in text ↑

salicylic acid · Ralstonia solanacearum · Nicotiana tabacum (tobacco)Positive and negative results

2 papers: 1 positive, 1 negative or no effect

1 in the opposite direction

  1. positive
See all 2 papers →

salicylic acid · Ralstonia solanacearum · Solanum lycopersicum (tomato)Results agree

7 papers: 7 positive, 0 negative or no effect

6 papers in the same direction as this paper

  1. positive
  2. positive
  3. positive

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.