Paper · 2001 · The Plant Cell

Hydrogen Peroxide Acts as a Second Messenger for the Induction of Defense Genes in Tomato Plants in Response to Wounding, Systemin, and Methyl Jasmonate

Martha L. Orozco-Cárdenas; Javier Narváez-Vásquez; Clarence A. Ryan

11
claims
19
verbatim quotes
891
citations
3
research areas
✓
Open access

Abstract

The systemic accumulation of both hydrogen peroxide (H(2)O(2)) and proteinase inhibitor proteins in tomato leaves in response to wounding was inhibited by the NADPH oxidase inhibitors diphenylene iodonium (DPI), imidazole, and pyridine. The expression of several defense genes in response to wounding, systemin, oligosaccharides, and methyl jasmonate also was inhibited by DPI. These genes, including those of four proteinase inhibitors and polyphenol oxidase, are expressed within 4 to 12 hr after wounding. However, DPI did not inhibit the wound-inducible expression of genes encoding prosystemin, lipoxygenase, and allene oxide synthase, which are associated with the octadecanoid signaling pathway and are expressed 0.5 to 2 hr after wounding. Accordingly, treatment of plants with the H(2)O(2)-generating enzyme glucose oxidase plus glucose resulted in the induction of only the later-expressed defensive genes and not the early-expressed signaling-related genes. H(2)O(2) was cytochemically detected in the cell walls of vascular parenchyma cells and spongy mesophyll cells within 4 hr after wounding of wild-type tomato leaves, but not earlier. The cumulative results suggest that active oxygen species are generated near cell walls of vascular bundle cells by oligogalacturonide fragments produced by wound-inducible polygalacturonase and that the resulting H(2)O(2) acts as a second messenger for the activation of defense genes in mesophyll cells. These data provide a rationale for the sequential, coordinated, and functional roles of systemin, jasmonic acid, oligogalacturonides, and H(2)O(2) signals for systemic signaling in tomato plants in response to wounding.

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Claims 11

Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

NADPH oxidase inhibitors blocked systemic hydrogen peroxide accumulation after wounding.

Organ / stage
leavese0
Treatment
NADPH oxidase inhibitors diphenylene iodonium (DPI), imidazole, and pyridinee0
Outcome
systemic accumulation of both hydrogen peroxide (H(2)O(2))e0
Direction
inhibitede0

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

“The systemic accumulation of both hydrogen peroxide (H(2)O(2)) and proteinase inhibitor proteins in tomato leaves in response to wounding was inhibited by the NADPH oxidase inhibitors diphenylene iodonium (DPI), imidazole, and pyridine.”

✓ located verbatim in the source · abstract, characters 0–236 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

NADPH oxidase inhibitors blocked systemic proteinase inhibitor accumulation after wounding.

Treatment
NADPH oxidase inhibitors diphenylene iodonium (DPI), imidazole, and pyridinee0
Outcome
proteinase inhibitor proteinse0
Direction
inhibitede0

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

“The systemic accumulation of both hydrogen peroxide (H(2)O(2)) and proteinase inhibitor proteins in tomato leaves in response to wounding was inhibited by the NADPH oxidase inhibitors diphenylene iodonium (DPI), imidazole, and pyridine.”

✓ located verbatim in the source · abstract, characters 0–236 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

DPI inhibited defense gene expression in response to wounding, systemin, oligosaccharides and methyl jasmonate.

Treatment
DPIe0
Outcome
expression of several defense genese0
Direction
inhibitede0

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

“The expression of several defense genes in response to wounding, systemin, oligosaccharides, and methyl jasmonate also was inhibited by DPI.”

✓ located verbatim in the source · abstract, characters 237–377 · show in text ↑
t0

“tomato”

✓ located after whitespace/quote normalisation · title, characters 83–89 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Later defense genes were expressed 4 to 12 hours after wounding.

Gene
four proteinase inhibitors and polyphenol oxidasee0
Outcome
expressede0
Value
4 to 12 hre0

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

“These genes, including those of four proteinase inhibitors and polyphenol oxidase, are expressed within 4 to 12 hr after wounding.”

✓ located verbatim in the source · abstract, characters 378–508 · show in text ↑
t0

“tomato”

✓ located after whitespace/quote normalisation · title, characters 83–89 · show in text ↑
Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

DPI did not inhibit early wound inducible signaling genes.

Treatment
DPIe0
Outcome
wound-inducible expression of genes encoding prosystemin, lipoxygenase, and allene oxide synthasee0
Direction
did not inhibite0

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

“DPI did not inhibit the wound-inducible expression of genes encoding prosystemin, lipoxygenase, and allene oxide synthase”

✓ located verbatim in the source · abstract, characters 518–639 · show in text ↑
t0

“tomato”

✓ located after whitespace/quote normalisation · title, characters 83–89 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Early wound signaling genes were expressed 0.5 to 2 hours after wounding.

Outcome
expressede0
Value
0.5 to 2 hre0

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

“are expressed 0.5 to 2 hr after wounding.”

✓ located verbatim in the source · abstract, characters 706–747 · show in text ↑
t0

“tomato”

✓ located after whitespace/quote normalisation · title, characters 83–89 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Glucose oxidase plus glucose induced later defense genes.

Treatment
glucose oxidase plus glucosee0
Outcome
later-expressed defensive genese0
Direction
inductione0

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

“treatment of plants with the H(2)O(2)-generating enzyme glucose oxidase plus glucose resulted in the induction of only the later-expressed defensive genes and not the early-expressed signaling-related genes.”

✓ located verbatim in the source · abstract, characters 761–968 · show in text ↑
t0

“tomato”

✓ located after whitespace/quote normalisation · title, characters 83–89 · show in text ↑
Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

Glucose oxidase plus glucose did not induce early signaling genes.

Treatment
glucose oxidase plus glucosee0
Outcome
early-expressed signaling-related genese0
Direction
note0

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

“treatment of plants with the H(2)O(2)-generating enzyme glucose oxidase plus glucose resulted in the induction of only the later-expressed defensive genes and not the early-expressed signaling-related genes.”

✓ located verbatim in the source · abstract, characters 761–968 · show in text ↑
t0

“tomato”

✓ located after whitespace/quote normalisation · title, characters 83–89 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Hydrogen peroxide was detected in vascular parenchyma and spongy mesophyll cell walls within four hours after wounding.

Organ / stage
cell walls of vascular parenchyma cells and spongy mesophyll cellse0
Outcome
H(2)O(2) was cytochemically detectede0
Value
4 hre0

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

“H(2)O(2) was cytochemically detected in the cell walls of vascular parenchyma cells and spongy mesophyll cells within 4 hr after wounding of wild-type tomato leaves, but not earlier.”

✓ located verbatim in the source · abstract, characters 969–1151 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

The authors infer that wound produced oligogalacturonides generate active oxygen near vascular cell walls.

Outcome
active oxygen species are generated near cell walls of vascular bundle cellse0
Qualifier
oligogalacturonide fragments produced by wound-inducible polygalacturonasee0

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

“active oxygen species are generated near cell walls of vascular bundle cells by oligogalacturonide fragments produced by wound-inducible polygalacturonase”

✓ located verbatim in the source · abstract, characters 1188–1342 · show in text ↑
t0

“tomato”

✓ located after whitespace/quote normalisation · title, characters 83–89 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

The authors infer hydrogen peroxide acts as a second messenger activating mesophyll defense genes.

Outcome
activation of defense genes in mesophyll cellse0
Qualifier
H(2)O(2) acts as a second messengere0

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

“the resulting H(2)O(2) acts as a second messenger for the activation of defense genes in mesophyll cells.”

✓ located verbatim in the source · abstract, characters 1352–1457 · show in text ↑
t0

“tomato”

✓ located after whitespace/quote normalisation · title, characters 83–89 · show in text ↑

dibenziodolium · molecular: expression · Solanum lycopersicum (tomato)Results agree

2 papers: 0 positive, 2 negative or no effect

1 paper in the same direction as this paper

  1. negative
See all 2 papers →

glucose · molecular: expression · Solanum lycopersicum (tomato)Results agree

4 papers: 4 positive, 0 negative or no effect

3 papers in the same direction as this paper

  1. positive
  2. positive
  3. positive
See all 4 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.