Paper · 2024 · PLANT PHYSIOLOGY

Related type 2C protein phosphatases Pic3 and Pic12 negatively regulate immunity in tomato to Pseudomonas syringae

Fan Xia; Ning Zhang; Renee E Smith; et al.

8
claims
17
verbatim quotes
2
citations
2
research areas
—
Not open access

Abstract

Type 2C protein phosphatases (PP2Cs) constitute a large family in most plant species, but relatively few of them have been implicated in immunity. To identify and characterize PP2C phosphatases that affect tomato (Solanum lycopersicum) immunity, we generated loss-of-function mutations in 11 PP2C-encoding genes whose expression is altered in response to immune elicitors or pathogens. We report that 2 closely related PP2C phosphatases, PP2C immunity-associated candidate 3 (Pic3) and Pic12, are involved in regulating resistance to the bacterial pathogen Pseudomonas syringae pv. tomato (Pst). Loss-of-function mutations in Pic3 led to enhanced resistance to Pst in older but not younger leaves, whereas such mutations in Pic12 resulted in enhanced resistance in both older and younger leaves. Overexpression of Pic3 and Pic12 proteins in leaves of Nicotiana benthamiana inhibited resistance to Pst, and this effect was dependent on Pic3/12 phosphatase activity and an N-terminal palmitoylation motif associated with localization to the cell periphery. Pic3, but not Pic12, had a slight negative effect on flagellin-associated reactive oxygen species generation, although their involvement in the response to Pst appeared independent of flagellin. RNA-sequencing analysis of Rio Grande (RG)-PtoR wild-type plants and 2 independent RG-pic3 mutants revealed that the enhanced disease resistance in RG-pic3 older leaves is associated with increased transcript abundance of multiple defense-related genes. RG-pic3/RG-pic12 double-mutant plants exhibited stronger disease resistance than RG-pic3 or RG-pic12 single mutants. Together, our results reveal that Pic3 and Pic12 negatively regulate tomato immunity in an additive manner through flagellin-independent pathways.

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Claims 8

Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Pic3 loss enhanced resistance to Pst in older tomato leaves but not younger leaves.

Organ / stage
older but not younger leavese0
Treatment
Loss-of-function mutations in Pic3e0
Interactor
Pseudomonas syringae pv. tomatoPseudomonas syringae pv. tomatoe2pathogen
Gene
Pic3e0
Outcome
resistance to Pste0
Direction
enhancede0

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 ↗
Pseudomonas syringae pv. tomato
Pseudomonas syringae pv. tomato · InteractorHoward F. Schwartz · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“Loss-of-function mutations in Pic3 led to enhanced resistance to Pst in older but not younger leaves”

✓ located verbatim in the source · abstract, characters 596–696 · show in text ↑
e1

“tomato (Solanum lycopersicum) immunity”

✓ located verbatim in the source · abstract, characters 206–244 · show in text ↑
e2

“bacterial pathogen Pseudomonas syringae pv. tomato (Pst)”

✓ located verbatim in the source · abstract, characters 538–594 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Pic12 loss enhanced Pst resistance in older and younger tomato leaves.

Organ / stage
both older and younger leavese0
Treatment
mutations in Pic12e0
Interactor
Pseudomonas syringae pv. tomatoPseudomonas syringae pv. tomatoe2pathogen
Gene
Pic12e0
Outcome
resistancee0
Direction
enhancede0

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 ↗
Pseudomonas syringae pv. tomato
Pseudomonas syringae pv. tomato · InteractorHoward F. Schwartz · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“mutations in Pic12 resulted in enhanced resistance in both older and younger leaves”

✓ located verbatim in the source · abstract, characters 711–794 · show in text ↑
e1

“tomato (Solanum lycopersicum) immunity”

✓ located verbatim in the source · abstract, characters 206–244 · show in text ↑
e2

“bacterial pathogen Pseudomonas syringae pv. tomato (Pst)”

✓ located verbatim in the source · abstract, characters 538–594 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Overexpression of Pic3 inhibited Pst resistance in Nicotiana leaves.

Taxon
Nicotiana benthamianaNicotiana benthamianae0
Organ / stage
leavese0
Treatment
Overexpression of Pic3e0
Interactor
Pseudomonas syringae pv. tomatoPseudomonas syringae pv. tomatoe1pathogen
Gene
Pic3e0
Outcome
resistance to Pste0
Direction
inhibitede0

Not reportedComparator

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

Nicotiana benthamiana
Nicotiana benthamiana · TaxonCharles Andres · CC BY-SA 3.0 · Wikimedia Commons ↗
Pseudomonas syringae pv. tomato
Pseudomonas syringae pv. tomato · InteractorHoward F. Schwartz · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“Overexpression of Pic3 and Pic12 proteins in leaves of Nicotiana benthamiana inhibited resistance to Pst”

✓ located verbatim in the source · abstract, characters 796–900 · show in text ↑
e1

“bacterial pathogen Pseudomonas syringae pv. tomato (Pst)”

✓ located verbatim in the source · abstract, characters 538–594 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Overexpression of Pic12 inhibited Pst resistance in Nicotiana leaves.

Taxon
Nicotiana benthamianaNicotiana benthamianae0
Organ / stage
leavese0
Treatment
Overexpression of Pic3 and Pic12 proteinse0
Interactor
Pseudomonas syringae pv. tomatoPseudomonas syringae pv. tomatoe1pathogen
Gene
Pic12e0
Outcome
resistance to Pste0
Direction
inhibitede0

Not reportedComparator

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

Nicotiana benthamiana
Nicotiana benthamiana · TaxonCharles Andres · CC BY-SA 3.0 · Wikimedia Commons ↗
Pseudomonas syringae pv. tomato
Pseudomonas syringae pv. tomato · InteractorHoward F. Schwartz · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“Overexpression of Pic3 and Pic12 proteins in leaves of Nicotiana benthamiana inhibited resistance to Pst”

✓ located verbatim in the source · abstract, characters 796–900 · show in text ↑
e1

“bacterial pathogen Pseudomonas syringae pv. tomato (Pst)”

✓ located verbatim in the source · abstract, characters 538–594 · show in text ↑
Observationobservedoriginal resultnegativemeasured

Claim · model-written summary

Pic3 slightly reduced flagellin associated reactive oxygen species generation; Pic12 did not.

Gene
Pic3e0
Outcome
flagellin-associated reactive oxygen species generatione0
Direction
negative effecte0

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

“Pic3, but not Pic12, had a slight negative effect on flagellin-associated reactive oxygen species generation”

✓ located verbatim in the source · abstract, characters 1055–1163 · show in text ↑
e1

“tomato (Solanum lycopersicum) immunity”

✓ located verbatim in the source · abstract, characters 206–244 · show in text ↑
Associationobservedoriginal resultpositivemeasured

Claim · model-written summary

Enhanced resistance of older RG-pic3 leaves was associated with increased defense gene transcripts.

Material
RG-pic3e0
Organ / stage
older leavese0
Outcome
transcript abundance of multiple defense-related genese0
Direction
increasede0

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

“enhanced disease resistance in RG-pic3 older leaves is associated with increased transcript abundance of multiple defense-related genes”

✓ located verbatim in the source · abstract, characters 1367–1502 · show in text ↑
e1

“tomato (Solanum lycopersicum) immunity”

✓ located verbatim in the source · abstract, characters 206–244 · show in text ↑
Observationobservedoriginal resultpositivemeasured

Claim · model-written summary

RG-pic3/RG-pic12 double mutants had stronger disease resistance than either single mutant.

Material
RG-pic3/RG-pic12 double-mutante0
Outcome
disease resistancee0
Direction
strongere0
Comparator
RG-pic3 or RG-pic12 single mutantse0

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

“RG-pic3/RG-pic12 double-mutant plants exhibited stronger disease resistance than RG-pic3 or RG-pic12 single mutants”

✓ located verbatim in the source · abstract, characters 1504–1619 · show in text ↑
e1

“tomato (Solanum lycopersicum) immunity”

✓ located verbatim in the source · abstract, characters 206–244 · show in text ↑
Mechanismauthor interpretationoriginal resultnegativemeasured

Claim · model-written summary

Pic3 and Pic12 negatively regulate tomato immunity additively through flagellin independent pathways.

Gene
Pic3 and Pic12e0
Outcome
tomato immunitye0
Direction
negatively regulatee0
Qualifier
flagellin-independent pathwayse0

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

“Pic3 and Pic12 negatively regulate tomato immunity in an additive manner through flagellin-independent pathways”

✓ located verbatim in the source · abstract, characters 1655–1766 · show in text ↑

loss of function · Pseudomonas syringae pv. tomato · Solanum lycopersicum (tomato)Positive and negative results

10 papers: 4 positive, 6 negative or no effect

3 papers in the same direction as this paper · 6 in the opposite direction

  1. negative
  2. negative
  3. positive

6 papers more in this group

See all 10 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.