Paper · 2018 · Molecular Plant-Microbe Interactions

Mimicking the Host Regulation of Salicylic Acid: A Virulence Strategy by the Clubroot Pathogen Plasmodiophora brassicae

Mohammad Djavaheri; Lisong Ma; Daniel F. Klessig; et al.

13
claims
19
verbatim quotes
41
citations
3
research areas
✓
Open access

Abstract

The plant hormone salicylic acid (SA) plays a critical role in defense against biotrophic pathogens such as Plasmodiophora brassicae, which is an obligate pathogen of crucifer species and the causal agent of clubroot disease of canola (Brassica napus). P. brassicae encodes a protein, predicted to be secreted, with very limited homology to benzoic acid (BA)/SA-methyltransferase, designated PbBSMT. PbBSMT has a SA- and an indole-3-acetic acid-binding domain, which are also present in Arabidopsis thaliana BSMT1 (AtBSMT1) and, like AtBSMT1, has been shown to methylate BA and SA. In support of the hypothesis that P. brassicae uses PbBSMT to overcome SA-mediated defenses by converting SA into inactive methyl salicylate (MeSA), here, we show that PbBSMT suppresses local defense and provide evidence that PbBSMT is much more effective than AtBSMT1 at suppressing the levels of SA and its associated effects. Basal SA levels in Arabidopsis plants that constitutively overexpress PbBSMT compared with those in Arabidopsis wild-type Col-0 (WT) were reduced approximately 80% versus only a 50% reduction in plants overexpressing AtBSMT1. PbBSMT-overexpressing plants were more susceptible to P. brassicae than WT plants; they also were partially compromised in nonhost resistance to Albugo candida. In contrast, AtBSMT1-overexpressing plants were not more susceptible than WT to either P. brassicae or A. candida. Furthermore, transgenic Arabidopsis and tobacco plants overexpressing PbBSMT exhibited increased susceptibility to virulent Pseudomonas syringae pv. tomato DC3000 (DC3000) and virulent Pseudomonas syringae pv. tabaci, respectively. Gene-mediated resistance to DC3000/AvrRpt2 and tobacco mosaic virus (TMV) was also compromised in Arabidopsis and Nicotiana tabacum 'Xanthi-nc' plants overexpressing PbBSMT, respectively. Transient expression of PbBSMT or AtBSMT1 in lower leaves of N. tabacum Xanthi-nc resulted in systemic acquired resistance (SAR)-like enhanced resistance to TMV in the distal systemic leaves. Chimeric grafting experiments revealed that, similar to SAR, the development of a PbBSMT-mediated SAR-like phenotype was also dependent on the MeSA esterase activity of NtSABP2 in the systemic leaves. Collectively, these results strongly suggest that PbBSMT is a novel effector, which is secreted by P. brassicae into its host plant to deplete pathogen-induced SA accumulation.

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Claims 13

Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

PbBSMT suppressed local defense.

Taxon
ArabidopsisArabidopsise1
Treatment
PbBSMTe0
Interactor
Plasmodiophora brassicaePlasmodiophora brassicaet0pathogen
Gene
PbBSMTe0
Outcome
local defensee0
Direction
suppressese0

Not reportedComparator

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 ↗
Plasmodiophora brassicae
Plasmodiophora brassicae · InteractorRasbak · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“PbBSMT suppresses local defense”

✓ located verbatim in the source · abstract, characters 750–781 · show in text ↑
t0

“Plasmodiophora brassicae”

✓ located verbatim in the source · title, characters 95–119 · show in text ↑
e1

“Basal SA levels in Arabidopsis plants”

✓ located verbatim in the source · abstract, characters 911–948 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

PbBSMT overexpression reduced Arabidopsis basal SA by approximately 80% versus wild type.

Taxon
ArabidopsisArabidopsise0
Treatment
constitutively overexpress PbBSMTe0
Gene
PbBSMTe0
Outcome
Basal SA levelse0
Direction
reducede0
Value
approximately 80%e0
Comparator
Arabidopsis wild-type Col-0 (WT)e0

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 ↗

Verbatim

e0

“Basal SA levels in Arabidopsis plants that constitutively overexpress PbBSMT compared with those in Arabidopsis wild-type Col-0 (WT) were reduced approximately 80%”

✓ located verbatim in the source · abstract, characters 911–1074 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

AtBSMT1 overexpression reduced basal SA by 50%.

Taxon
ArabidopsisArabidopsise0
Treatment
overexpressing AtBSMT1e0
Gene
AtBSMT1e0
Outcome
SA levelse0
Direction
reductione0
Value
50%e0

Not reportedComparator

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 ↗

Verbatim

e0

“Basal SA levels in Arabidopsis plants that constitutively overexpress PbBSMT compared with those in Arabidopsis wild-type Col-0 (WT) were reduced approximately 80% versus only a 50% reduction in plants overexpressing AtBSMT1.”

✓ located verbatim in the source · abstract, characters 911–1136 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

PbBSMT overexpression increased Arabidopsis susceptibility to P. brassicae.

Taxon
ArabidopsisArabidopsist0
Treatment
PbBSMT-overexpressinge0
Interactor
P. brassicaee0pathogen
Gene
PbBSMTe0
Outcome
susceptible to P. brassicaee0
Direction
moree0
Comparator
WT plantse0

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 ↗

Verbatim

e0

“PbBSMT-overexpressing plants were more susceptible to P. brassicae than WT plants”

✓ located verbatim in the source · abstract, characters 1137–1218 · show in text ↑
t0

“Basal SA levels in Arabidopsis plants”

✓ located verbatim in the source · abstract, characters 911–948 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

PbBSMT overexpression partly compromised nonhost resistance to Albugo candida.

Taxon
ArabidopsisArabidopsist0
Treatment
PbBSMT-overexpressinge0
Interactor
Albugo candidaAlbugo candidae0pathogen
Outcome
nonhost resistance to Albugo candidae0
Direction
compromisede0

Not reportedComparator

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 ↗
Albugo candida
Albugo candida · InteractorPlant pests and diseases · CC0 · Wikimedia Commons ↗

Verbatim

e0

“PbBSMT-overexpressing plants were more susceptible to P. brassicae than WT plants; they also were partially compromised in nonhost resistance to Albugo candida.”

✓ located verbatim in the source · abstract, characters 1137–1297 · show in text ↑
t0

“Basal SA levels in Arabidopsis plants”

✓ located verbatim in the source · abstract, characters 911–948 · show in text ↑
Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

AtBSMT1 overexpression did not increase susceptibility to P. brassicae or A. candida.

Taxon
ArabidopsisArabidopsist0
Treatment
AtBSMT1-overexpressinge0
Interactor
P. brassicaee0pathogen
Second interactor
A. candidaAlbugo candidae0pathogen
Outcome
susceptiblee0
Direction
not moree0
Comparator
WTe0

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 ↗
Albugo candida
Albugo candida · Second interactorPlant pests and diseases · CC0 · Wikimedia Commons ↗

Verbatim

e0

“AtBSMT1-overexpressing plants were not more susceptible than WT to either P. brassicae or A. candida.”

✓ located verbatim in the source · abstract, characters 1311–1412 · show in text ↑
t0

“Basal SA levels in Arabidopsis plants”

✓ located verbatim in the source · abstract, characters 911–948 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

PbBSMT overexpression increased Arabidopsis susceptibility to Pseudomonas syringae pv. tomato DC3000.

Taxon
ArabidopsisArabidopsise0
Treatment
overexpressing PbBSMTe0
Interactor
Pseudomonas syringae pv. tomato DC3000Pseudomonas syringae pv. tomato str. DC3000e0pathogen
Outcome
susceptibilitye0
Direction
increasede0

Not reportedComparator

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 ↗

Verbatim

e0

“transgenic Arabidopsis and tobacco plants overexpressing PbBSMT exhibited increased susceptibility to virulent Pseudomonas syringae pv. tomato DC3000 (DC3000) and virulent Pseudomonas syringae pv. tabaci, respectively.”

✓ located verbatim in the source · abstract, characters 1426–1644 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

PbBSMT overexpression increased tobacco susceptibility to Pseudomonas syringae pv. tabaci.

Treatment
overexpressing PbBSMTe0
Interactor
Pseudomonas syringae pv. tabaciPseudomonas amygdali pv. tabacie0pathogen
Outcome
susceptibilitye0
Direction
increasede0

Not reportedComparator

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 ↗

Verbatim

e0

“transgenic Arabidopsis and tobacco plants overexpressing PbBSMT exhibited increased susceptibility to virulent Pseudomonas syringae pv. tomato DC3000 (DC3000) and virulent Pseudomonas syringae pv. tabaci, respectively.”

✓ located verbatim in the source · abstract, characters 1426–1644 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

PbBSMT compromised Arabidopsis gene-mediated resistance to DC3000/AvrRpt2.

Taxon
ArabidopsisArabidopsise0
Treatment
overexpressing PbBSMTe0
Interactor
DC3000e0pathogen
Outcome
Gene-mediated resistance to DC3000/AvrRpt2e0
Direction
compromisede0

Not reportedComparator

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 ↗

Verbatim

e0

“Gene-mediated resistance to DC3000/AvrRpt2 and tobacco mosaic virus (TMV) was also compromised in Arabidopsis and Nicotiana tabacum 'Xanthi-nc' plants overexpressing PbBSMT, respectively.”

✓ located verbatim in the source · abstract, characters 1645–1832 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

PbBSMT compromised tobacco resistance to TMV.

Taxon
Nicotiana tabacumNicotiana tabacume0
Material
Xanthi-nce0
Treatment
overexpressing PbBSMTe0
Interactor
tobacco mosaic virusTobacco mosaic viruse0pathogen
Outcome
resistance to DC3000/AvrRpt2 and tobacco mosaic virus (TMV)e0
Direction
compromisede0

Not reportedComparator

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 ↗
Tobacco mosaic virus
Tobacco mosaic virus · InteractorFrank Vincentz · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“Gene-mediated resistance to DC3000/AvrRpt2 and tobacco mosaic virus (TMV) was also compromised in Arabidopsis and Nicotiana tabacum 'Xanthi-nc' plants overexpressing PbBSMT, respectively.”

✓ located verbatim in the source · abstract, characters 1645–1832 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Transient PbBSMT expression in lower tobacco leaves enhanced distal resistance to TMV.

Taxon
N. tabacumNicotiana tabacume0
Treatment
Transient expression of PbBSMTe0
Interactor
TMVTobacco mosaic viruse0pathogen
Outcome
resistance to TMVe0
Direction
enhancede0

Not reportedComparator

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 ↗
Tobacco mosaic virus
Tobacco mosaic virus · InteractorFrank Vincentz · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“Transient expression of PbBSMT or AtBSMT1 in lower leaves of N. tabacum Xanthi-nc resulted in systemic acquired resistance (SAR)-like enhanced resistance to TMV in the distal systemic leaves.”

✓ located verbatim in the source · abstract, characters 1833–2024 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Transient AtBSMT1 expression in lower tobacco leaves enhanced distal resistance to TMV.

Taxon
N. tabacumNicotiana tabacume0
Treatment
AtBSMT1e0
Interactor
TMVTobacco mosaic viruse0pathogen
Outcome
resistance to TMVe0
Direction
enhancede0

Not reportedComparator

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 ↗
Tobacco mosaic virus
Tobacco mosaic virus · InteractorFrank Vincentz · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“Transient expression of PbBSMT or AtBSMT1 in lower leaves of N. tabacum Xanthi-nc resulted in systemic acquired resistance (SAR)-like enhanced resistance to TMV in the distal systemic leaves.”

✓ located verbatim in the source · abstract, characters 1833–2024 · show in text ↑
Mechanismobservedoriginal resultmeasured

Claim · model-written summary

PbBSMT-mediated SAR-like resistance depended on NtSABP2 MeSA esterase activity in systemic leaves.

Taxon
N. tabacumNicotiana tabacumt0
Organ / stage
systemic leavese0
Gene
NtSABP2e0
Outcome
PbBSMT-mediated SAR-like phenotypee0

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 ↗

Verbatim

e0

“the development of a PbBSMT-mediated SAR-like phenotype was also dependent on the MeSA esterase activity of NtSABP2 in the systemic leaves.”

✓ located verbatim in the source · abstract, characters 2086–2225 · show in text ↑
t0

“N. tabacum Xanthi-nc”

✓ located verbatim in the source · abstract, characters 1894–1914 · show in text ↑

overexpression · Tobacco mosaic virus · Nicotiana tabacum (tobacco)Positive and negative results

4 papers: 2 positive, 2 negative or no effect

1 paper in the same direction as this paper · 2 in the opposite direction

  1. positive
  2. positive
  3. no effect
See all 4 papers →

transgenic · Tobacco mosaic virus · Nicotiana tabacum (tobacco)Positive and negative results

12 papers: 11 positive, 1 negative or no effect

10 papers in the same direction as this paper · 1 in the opposite direction

  1. no effect
  2. positive
  3. positive

8 papers more in this group

See all 12 papers →

overexpression · molecular: expression · ArabidopsisPositive and negative results

55 papers: 41 positive, 14 negative or no effect

13 papers in the same direction as this paper · 41 in the opposite direction

  1. positive
  2. positive
  3. positive

51 papers more in this group

See all 55 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.