Paper · 2016 · The Plant Journal

Orchestration of hydrogen peroxide and nitric oxide in brassinosteroid‐mediated systemic virus resistance in Nicotiana benthamiana

Xing‐Guang Deng; Tong Zhu; Li‐Juan Zou; et al.

16
claims
30
verbatim quotes
129
citations
3
research areas
—
Not open access

Abstract

Brassinosteroids (BRs) play essential roles in modulating plant growth, development and stress responses. Here, involvement of BRs in plant systemic resistance to virus was studied. Treatment of local leaves in Nicotiana benthamiana with BRs induced virus resistance in upper untreated leaves, accompanied by accumulations of H2O2 and NO. Scavenging of H2O2 or NO in upper leaves blocked BR-induced systemic virus resistance. BR-induced systemic H2O2 accumulation was blocked by local pharmacological inhibition of NADPH oxidase or silencing of respiratory burst oxidase homolog gene NbRBOHB, but not by systemic NADPH oxidase inhibition or NbRBOHA silencing. Silencing of the nitrite-dependent nitrate reductase gene NbNR or systemic pharmacological inhibition of NR compromised BR-triggered systemic NO accumulation, while local inhibition of NR, silencing of NbNOA1 and inhibition of NOS had little effect. Moreover, we provide evidence that BR-activated H2O2 is required for NO synthesis. Pharmacological scavenging or genetic inhibiting of H2O2 generation blocked BR-induced systemic NO production, but BR-induced H2O2 production was not sensitive to NO scavengers or silencing of NbNR. Systemically applied sodium nitroprusside rescued BR-induced systemic virus defense in NbRBOHB-silenced plants, but H2O2 did not reverse the effect of NbNR silencing on BR-induced systemic virus resistance. Finally, we demonstrate that the receptor kinase BRI1(BR insensitive 1) is an upstream component in BR-mediated systemic defense signaling, as silencing of NbBRI1 compromised the BR-induced H2O2 and NO production associated with systemic virus resistance. Together, our pharmacological and genetic data suggest the existence of a signaling pathway leading to BR-mediated systemic virus resistance that involves local Respiratory Burst Oxidase Homolog B (RBOHB)-dependent H2O2 production and subsequent systemic NR-dependent NO generation.

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Claims 16

Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Local BR treatment induced resistance in untreated upper leaves.

Taxon
Nicotiana benthamianaNicotiana benthamianae0
Treatment
BRse0
Outcome
virus resistancee0
Direction
inducede0
Comparator
untreated leavese0

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 ↗

Verbatim

e0

“Treatment of local leaves in Nicotiana benthamiana with BRs induced virus resistance in upper untreated leaves”

✓ located verbatim in the source · abstract, characters 182–292 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

BR treatment accumulated H2O2 and NO in upper leaves.

Taxon
Nicotiana benthamianaNicotiana benthamianae0
Treatment
BRse0
Outcome
accumulations of H2O2 and NOe0
Direction
accumulationse0
Comparator
untreated leavese0

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 ↗

Verbatim

e0

“Treatment of local leaves in Nicotiana benthamiana with BRs induced virus resistance in upper untreated leaves, accompanied by accumulations of H2O2 and NO”

✓ located verbatim in the source · abstract, characters 182–337 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Scavenging H2O2 blocked BR induced systemic resistance.

Taxon
Nicotiana benthamianaNicotiana benthamianat0
Treatment
Scavenging of H2O2e0
Outcome
BR-induced systemic virus resistancee0
Direction
blockede0
Comparator
NOe0

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 ↗

Verbatim

e0

“Scavenging of H2O2 or NO in upper leaves blocked BR-induced systemic virus resistance”

✓ located verbatim in the source · abstract, characters 339–424 · show in text ↑
t0

“Nicotiana benthamiana”

✓ located verbatim in the source · title, characters 109–130 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Scavenging NO blocked BR induced systemic resistance.

Taxon
Nicotiana benthamianaNicotiana benthamianat0
Treatment
NOe0
Outcome
BR-induced systemic virus resistancee0
Direction
blockede0
Comparator
H2O2e0

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 ↗

Verbatim

e0

“Scavenging of H2O2 or NO in upper leaves blocked BR-induced systemic virus resistance”

✓ located verbatim in the source · abstract, characters 339–424 · show in text ↑
t0

“Nicotiana benthamiana”

✓ located verbatim in the source · title, characters 109–130 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Local NADPH oxidase inhibition blocked systemic H2O2 accumulation.

Taxon
Nicotiana benthamianaNicotiana benthamianat0
Treatment
local pharmacological inhibition of NADPH oxidasee0
Outcome
BR-induced systemic H2O2 accumulatione0
Direction
blockede0
Comparator
BR-inducede0

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 ↗

Verbatim

e0

“BR-induced systemic H2O2 accumulation was blocked by local pharmacological inhibition of NADPH oxidase”

✓ located verbatim in the source · abstract, characters 426–528 · show in text ↑
t0

“Nicotiana benthamiana”

✓ located verbatim in the source · title, characters 109–130 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

NbRBOHB silencing blocked systemic H2O2 accumulation.

Taxon
Nicotiana benthamianaNicotiana benthamianat0
Treatment
silencinge0
Gene
NbRBOHBe0
Outcome
silencing of respiratory burst oxidase homolog gene NbRBOHBe0

Not reportedComparatorDirection

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 ↗

Verbatim

e0

“silencing of respiratory burst oxidase homolog gene NbRBOHB”

✓ located verbatim in the source · abstract, characters 532–591 · show in text ↑
t0

“Nicotiana benthamiana”

✓ located verbatim in the source · title, characters 109–130 · show in text ↑
Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

Systemic NADPH oxidase inhibition did not block H2O2 accumulation.

Taxon
Nicotiana benthamianaNicotiana benthamianat0
Treatment
systemic NADPH oxidase inhibitione0
Outcome
systemic NADPH oxidase inhibitione0
Direction
note0

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 ↗

Verbatim

e0

“but not by systemic NADPH oxidase inhibition or NbRBOHA silencing”

✓ located verbatim in the source · abstract, characters 593–658 · show in text ↑
t0

“Nicotiana benthamiana”

✓ located verbatim in the source · title, characters 109–130 · show in text ↑
Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

NbRBOHA silencing did not block H2O2 accumulation.

Taxon
Nicotiana benthamianaNicotiana benthamianat0
Treatment
silencinge0
Gene
NbRBOHAe0
Outcome
NbRBOHA silencinge0
Direction
note0

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 ↗

Verbatim

e0

“but not by systemic NADPH oxidase inhibition or NbRBOHA silencing”

✓ located verbatim in the source · abstract, characters 593–658 · show in text ↑
t0

“Nicotiana benthamiana”

✓ located verbatim in the source · title, characters 109–130 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

NbNR silencing compromised systemic NO accumulation.

Taxon
Nicotiana benthamianaNicotiana benthamianat0
Treatment
Silencinge0
Gene
NbNRe0
Outcome
BR-triggered systemic NO accumulatione0
Direction
compromisede0

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 ↗

Verbatim

e0

“Silencing of the nitrite-dependent nitrate reductase gene NbNR or systemic pharmacological inhibition of NR compromised BR-triggered systemic NO accumulation”

✓ located verbatim in the source · abstract, characters 660–817 · show in text ↑
t0

“Nicotiana benthamiana”

✓ located verbatim in the source · title, characters 109–130 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Systemic NR inhibition compromised systemic NO accumulation.

Taxon
Nicotiana benthamianaNicotiana benthamianat0
Treatment
systemic pharmacological inhibition of NRe0
Outcome
BR-triggered systemic NO accumulatione0
Direction
compromisede0

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 ↗

Verbatim

e0

“Silencing of the nitrite-dependent nitrate reductase gene NbNR or systemic pharmacological inhibition of NR compromised BR-triggered systemic NO accumulation”

✓ located verbatim in the source · abstract, characters 660–817 · show in text ↑
t0

“Nicotiana benthamiana”

✓ located verbatim in the source · title, characters 109–130 · show in text ↑
Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

Local NR inhibition, NbNOA1 silencing and NOS inhibition had little effect.

Taxon
Nicotiana benthamianaNicotiana benthamianat0
Treatment
local inhibition of NRe0
Outcome
little effecte0
Direction
little effecte0

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 ↗

Verbatim

e0

“while local inhibition of NR, silencing of NbNOA1 and inhibition of NOS had little effect”

✓ located verbatim in the source · abstract, characters 819–908 · show in text ↑
t0

“Nicotiana benthamiana”

✓ located verbatim in the source · title, characters 109–130 · show in text ↑
Mechanismobservedoriginal resultnegativemeasured

Claim · model-written summary

H2O2 generation was needed for BR induced NO production.

Taxon
Nicotiana benthamianaNicotiana benthamianat0
Outcome
BR-induced systemic NO productione0
Qualifier
H2O2 generatione0

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 ↗

Verbatim

e0

“Pharmacological scavenging or genetic inhibiting of H2O2 generation blocked BR-induced systemic NO production”

✓ located verbatim in the source · abstract, characters 993–1102 · show in text ↑
t0

“Nicotiana benthamiana”

✓ located verbatim in the source · title, characters 109–130 · show in text ↑
Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

NO scavenging or NbNR silencing did not affect BR induced H2O2 production.

Taxon
Nicotiana benthamianaNicotiana benthamianat0
Treatment
NO scavengerse0
Outcome
BR-induced H2O2 productione0
Direction
not sensitivee0

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 ↗

Verbatim

e0

“BR-induced H2O2 production was not sensitive to NO scavengers or silencing of NbNR”

✓ located verbatim in the source · abstract, characters 1108–1190 · show in text ↑
t0

“Nicotiana benthamiana”

✓ located verbatim in the source · title, characters 109–130 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Sodium nitroprusside restored systemic virus defense in NbRBOHB silenced plants.

Taxon
Nicotiana benthamianaNicotiana benthamianat0
Treatment
sodium nitroprussidee0
Outcome
BR-induced systemic virus defensee0
Direction
rescuede0
Comparator
NbRBOHB-silenced plantse0

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 ↗

Verbatim

e0

“Systemically applied sodium nitroprusside rescued BR-induced systemic virus defense in NbRBOHB-silenced plants”

✓ located verbatim in the source · abstract, characters 1192–1302 · show in text ↑
t0

“Nicotiana benthamiana”

✓ located verbatim in the source · title, characters 109–130 · show in text ↑
Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

H2O2 did not reverse the effect of NbNR silencing.

Taxon
Nicotiana benthamianaNicotiana benthamianat0
Treatment
H2O2e0
Outcome
BR-induced systemic virus resistancee0
Direction
did not reversee0
Comparator
NbNR silencinge0

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 ↗

Verbatim

e0

“H2O2 did not reverse the effect of NbNR silencing on BR-induced systemic virus resistance”

✓ located verbatim in the source · abstract, characters 1308–1397 · show in text ↑
t0

“Nicotiana benthamiana”

✓ located verbatim in the source · title, characters 109–130 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

NbBRI1 silencing compromised BR induced H2O2 and NO production.

Taxon
Nicotiana benthamianaNicotiana benthamianat0
Treatment
silencinge0
Gene
NbBRI1e0
Outcome
BR-induced H2O2 and NO productione0
Direction
compromisede0

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 ↗

Verbatim

e0

“silencing of NbBRI1 compromised the BR-induced H2O2 and NO production associated with systemic virus resistance”

✓ located verbatim in the source · abstract, characters 1542–1653 · show in text ↑
t0

“Nicotiana benthamiana”

✓ located verbatim in the source · title, characters 109–130 · show in text ↑

nitric oxide · disease · Nicotiana benthamianaResults 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 →

class · disease · Nicotiana benthamianaPositive and negative results

2 papers: 1 positive, 1 negative or no effect

1 in the opposite direction

  1. negative
See all 2 papers →

loss of function · physiology: oxidative · Nicotiana benthamianaPositive and negative results

16 papers: 6 positive, 10 negative or no effect

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

  1. positive
  2. positive
  3. positive

12 papers more in this group

See all 16 papers →

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

35 papers: 10 positive, 25 negative or no effect

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

  1. negative
  2. positive
  3. positive

31 papers more in this group

See all 35 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.