Paper · 2018 · PLoS Pathogens

The Xanthomonas euvesicatoria type III effector XopAU is an active protein kinase that manipulates plant MAP kinase signaling

Doron Teper; Anil Madhusoodana Girija; Eran Bosis; et al.

14
claims
29
verbatim quotes
46
citations
2
research areas
✓
Open access · cc-by

Abstract

The Gram-negative bacterium Xanthomonas euvesicatoria (Xe) is the causal agent of bacterial spot disease of pepper and tomato. Xe delivers effector proteins into host cells through the type III secretion system to promote disease. Here, we show that the Xe effector XopAU, which is conserved in numerous Xanthomonas species, is a catalytically active protein kinase and contributes to the development of disease symptoms in pepper plants. Agrobacterium-mediated expression of XopAU in host and non-host plants activated typical defense responses, including MAP kinase phosphorylation, accumulation of pathogenesis-related (PR) proteins and elicitation of cell death, that were dependent on the kinase activity of the effector. XopAU-mediated cell death was not dependent on early signaling components of effector-triggered immunity and was also observed when the effector was delivered into pepper leaves by Xanthomonas campestris pv. campestris, but not by Xe. Protein-protein interaction studies in yeast and in planta revealed that XopAU physically interacts with components of plant immunity-associated MAP kinase cascades. Remarkably, XopAU directly phosphorylated MKK2 in vitro and enhanced its phosphorylation at multiple sites in planta. Consistent with the notion that MKK2 is a target of XopAU, silencing of the MKK2 homolog or overexpression of the catalytically inactive mutant MKK2K99R in N. benthamiana plants reduced XopAU-mediated cell death and MAPK phosphorylation. Furthermore, yeast co-expressing XopAU and MKK2 displayed reduced growth and this phenotype was dependent on the kinase activity of both proteins. Together, our results support the conclusion that XopAU contributes to Xe disease symptoms in pepper plants and manipulates host MAPK signaling through phosphorylation and activation of MKK2.

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Claims 14

Observationobservedoriginal resultmeasured

Claim · model-written summary

XopAU is a catalytically active protein kinase.

Taxon
pepper plantse1
Interactor
Xanthomonas speciesXanthomonase0pathogen
Gene
XopAUe0
Outcome
catalytically active protein kinasee0

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

Xanthomonas
Xanthomonas · Interactor · picture from its Wikimedia Commons categoryHoward F. Schwartz, Colorado State University, Bugwood.org · CC BY 3.0 · Wikimedia Commons ↗

Verbatim

e0

“the Xe effector XopAU, which is conserved in numerous Xanthomonas species, is a catalytically active protein kinase”

✓ located verbatim in the source · abstract, characters 250–365 · show in text ↑
t0

“plant MAP kinase signaling”

✓ located verbatim in the source · title, characters 99–125 · show in text ↑
e1

“contributes to the development of disease symptoms in pepper plants”

✓ located verbatim in the source · abstract, characters 370–437 · show in text ↑
Observationobservedoriginal resultnegativemeasured

Claim · model-written summary

XopAU contributes to disease symptoms in pepper.

Taxon
pepper plantse0
Outcome
disease symptomse0

Verbatim

e0

“contributes to the development of disease symptoms in pepper plants”

✓ located verbatim in the source · abstract, characters 370–437 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

XopAU expression activated MAP kinase phosphorylation in host and non-host plants.

Taxon
plantsViridiplantaee0
Treatment
Agrobacterium-mediated expression of XopAUe0
Gene
XopAUe0
Outcome
MAP kinase phosphorylatione0
Direction
activatede0

Not reportedComparator

Verbatim

e0

“Agrobacterium-mediated expression of XopAU in host and non-host plants activated typical defense responses, including MAP kinase phosphorylation”

✓ located verbatim in the source · abstract, characters 439–583 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

XopAU expression induced accumulation of PR proteins.

Taxon
plantsViridiplantaee0
Treatment
Agrobacterium-mediated expression of XopAUe0
Gene
XopAUe0
Outcome
accumulation of pathogenesis-related (PR) proteinse0
Direction
accumulatione0

Not reportedComparator

Verbatim

e0

“Agrobacterium-mediated expression of XopAU in host and non-host plants activated typical defense responses, including MAP kinase phosphorylation, accumulation of pathogenesis-related (PR) proteins and elicitation of cell death”

✓ located verbatim in the source · abstract, characters 439–665 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

XopAU expression elicited cell death dependent on kinase activity.

Taxon
pepper plantse1
Treatment
kinase activity of the effectore0
Outcome
cell deathe0

Not reportedComparatorDirection

Verbatim

e0

“elicitation of cell death, that were dependent on the kinase activity of the effector”

✓ located verbatim in the source · abstract, characters 640–725 · show in text ↑
t0

“plant MAP kinase signaling”

✓ located verbatim in the source · title, characters 99–125 · show in text ↑
e1

“contributes to the development of disease symptoms in pepper plants”

✓ located verbatim in the source · abstract, characters 370–437 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

XopAU cell death was independent of early effector-triggered immunity signaling components.

Taxon
pepper plantse1
Gene
XopAUe0
Outcome
cell deathe0

Verbatim

e0

“XopAU-mediated cell death was not dependent on early signaling components of effector-triggered immunity”

✓ located verbatim in the source · abstract, characters 727–831 · show in text ↑
t0

“plant MAP kinase signaling”

✓ located verbatim in the source · title, characters 99–125 · show in text ↑
e1

“contributes to the development of disease symptoms in pepper plants”

✓ located verbatim in the source · abstract, characters 370–437 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

XopAU delivered by Xanthomonas campestris pv. campestris induced cell death in pepper leaves.

Taxon
peppere0
Treatment
delivered into pepper leaves by Xanthomonas campestris pv. campestrise0
Interactor
Xanthomonas campestris pv. campestrisXanthomonas campestris pv. campestrise0pathogen
Outcome
cell deathe0
Comparator
Xee0

Not reportedDirection

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

Xanthomonas campestris pv. campestris
Xanthomonas campestris pv. campestris · InteractorDavid B. Langston · CC BY 3.0 · Wikimedia Commons ↗

Verbatim

e0

“XopAU-mediated cell death was not dependent on early signaling components of effector-triggered immunity and was also observed when the effector was delivered into pepper leaves by Xanthomonas campestris pv. campestris, but not by Xe”

✓ located verbatim in the source · abstract, characters 727–960 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

XopAU interacted physically with components of plant immunity MAP kinase cascades.

Taxon
plante0
Gene
XopAUe0
Outcome
interacts with components of plant immunity-associated MAP kinase cascadese0

Verbatim

e0

“XopAU physically interacts with components of plant immunity-associated MAP kinase cascades”

✓ located verbatim in the source · abstract, characters 1035–1126 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

XopAU phosphorylated MKK2 in vitro.

Taxon
pepper plantse1
Gene
MKK2e0
Outcome
phosphorylated MKK2e0
Setting
in vitroe0

Verbatim

e0

“XopAU directly phosphorylated MKK2 in vitro”

✓ located verbatim in the source · abstract, characters 1140–1183 · show in text ↑
t0

“plant MAP kinase signaling”

✓ located verbatim in the source · title, characters 99–125 · show in text ↑
e1

“contributes to the development of disease symptoms in pepper plants”

✓ located verbatim in the source · abstract, characters 370–437 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

XopAU enhanced MKK2 phosphorylation at multiple sites in planta.

Taxon
pepper plantse1
Gene
MKK2e2
Outcome
phosphorylatione0
Direction
enhancede0

Verbatim

e0

“enhanced its phosphorylation at multiple sites in planta”

✓ located verbatim in the source · abstract, characters 1188–1244 · show in text ↑
t0

“plant MAP kinase signaling”

✓ located verbatim in the source · title, characters 99–125 · show in text ↑
e1

“contributes to the development of disease symptoms in pepper plants”

✓ located verbatim in the source · abstract, characters 370–437 · show in text ↑
e2

“XopAU directly phosphorylated MKK2 in vitro”

✓ located verbatim in the source · abstract, characters 1140–1183 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Silencing the MKK2 homolog reduced XopAU cell death and MAPK phosphorylation in N. benthamiana.

Taxon
N. benthamianae0
Treatment
silencing of the MKK2 homologe0
Gene
MKK2 homologe0
Outcome
XopAU-mediated cell death and MAPK phosphorylatione0
Direction
reducede0

Not reportedComparator

Verbatim

e0

“silencing of the MKK2 homolog or overexpression of the catalytically inactive mutant MKK2K99R in N. benthamiana plants reduced XopAU-mediated cell death and MAPK phosphorylation”

✓ located verbatim in the source · abstract, characters 1305–1482 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

MKK2K99R overexpression reduced XopAU cell death and MAPK phosphorylation in N. benthamiana.

Taxon
N. benthamianae0
Treatment
overexpression of the catalytically inactive mutant MKK2K99Re0
Gene
MKK2K99Re0
Outcome
XopAU-mediated cell death and MAPK phosphorylatione0
Direction
reducede0

Not reportedComparator

Verbatim

e0

“overexpression of the catalytically inactive mutant MKK2K99R in N. benthamiana plants reduced XopAU-mediated cell death and MAPK phosphorylation”

✓ located verbatim in the source · abstract, characters 1338–1482 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

XopAU and MKK2 coexpression reduced yeast growth in a kinase dependent manner.

Taxon
pepper plantse1
Gene
XopAU and MKK2e0
Outcome
yeast co-expressing XopAU and MKK2 displayed reduced growthe0
Direction
reducede0

Verbatim

e0

“yeast co-expressing XopAU and MKK2 displayed reduced growth and this phenotype was dependent on the kinase activity of both proteins”

✓ located verbatim in the source · abstract, characters 1497–1629 · show in text ↑
t0

“plant MAP kinase signaling”

✓ located verbatim in the source · title, characters 99–125 · show in text ↑
e1

“contributes to the development of disease symptoms in pepper plants”

✓ located verbatim in the source · abstract, characters 370–437 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

The authors conclude that XopAU manipulates host MAPK signaling by phosphorylation and activation of MKK2.

Taxon
pepper plantse1
Gene
MKK2e0
Outcome
host MAPK signalinge0
Qualifier
phosphorylation and activation of MKK2e0

Verbatim

e0

“manipulates host MAPK signaling through phosphorylation and activation of MKK2”

✓ located verbatim in the source · abstract, characters 1743–1821 · show in text ↑
t0

“plant MAP kinase signaling”

✓ located verbatim in the source · title, characters 99–125 · show in text ↑
e1

“contributes to the development of disease symptoms in pepper plants”

✓ located verbatim in the source · abstract, characters 370–437 · show in text ↑

transgenic · molecular: expression · Viridiplantae (plants)Positive and negative results

4 papers: 1 positive, 3 negative or no effect

2 in the opposite direction · 1 reporting no difference from an alternative

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

loss of function · molecular: expression · Nicotiana benthamianaPositive and negative results

43 papers: 19 positive, 24 negative or no effect

18 papers in the same direction as this paper · 24 in the opposite direction

  1. negative
  2. negative
  3. negative

39 papers more in this group

See all 43 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.