Paper · 2008 · The Plant Cell

Spermidine Exodus and Oxidation in the Apoplast Induced by Abiotic Stress Is Responsible for H2O2 Signatures That Direct Tolerance Responses in Tobacco

Panagiotis N. Moschou; Konstantinos A. Paschalidis; Ioannis D. Delis; et al.

10
claims
25
verbatim quotes
321
citations
1
research areas
✓
Open access

Abstract

Polyamines (PAs) exert a protective effect against stress challenges, but their molecular role in this remains speculative. In order to detect the signaling role of apoplastic PA-derived hydrogen peroxide (H2O2) under abiotic stress, we developed a series of tobacco (Nicotiana tabacum cv Xanthi) transgenic plants overexpressing or downregulating apoplastic polyamine oxidase (PAO; S-pao and A-pao plants, respectively) or downregulating S-adenosyl-l-methionine decarboxylase (samdc plants). Upon salt stress, plants secreted spermidine (Spd) into the apoplast, where it was oxidized by the apoplastic PAO, generating H2O2. A-pao plants accumulated less H2O2 and exhibited less programmed cell death (PCD) than did wild-type plants, in contrast with S-pao and samdc downregulating plants. Induction of either stress-responsive genes or PCD was dependent on the level of Spd-derived apoplastic H2O2. Thus, in wild-type and A-pao plants, stress-responsive genes were efficiently induced, although in the latter at a lower rate, while S-pao plants, with higher H2O2 levels, failed to accumulate stress-responsive mRNAs, inducing PCD instead. Furthermore, decreasing intracellular PAs, while keeping normal apoplastic Spd oxidation, as in samdc downregulating transgenic plants, caused enhanced salinity-induced PCD. These results reveal that salinity induces the exodus of Spd into the apoplast, where it is catabolized by PAO, producing H2O2. The accumulated H2O2 results in the induction of either tolerance responses or PCD, depending also on the levels of intracellular PAs.

Abstract from the paper’s OpenAlex record, shown for indexing and research. Copyright remains with the authors or the publisher. Read at the source ↗

The text the model read, with the source record’s inline markup (italics, sub- and superscripts) rendered and its character entities decoded; quote offsets refer to the raw text.

Claims 10

Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

A-pao tobacco plants accumulated less H2O2 than wild-type plants under salt stress.

Material
A-pao plantse1
Treatment
salt stresse2
Outcome
H2O2e1
Direction
lesse1
Comparator
wild-type plantse1

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

“we developed a series of tobacco (Nicotiana tabacum cv Xanthi) transgenic plants overexpressing or downregulating apoplastic polyamine oxidase (PAO; S-pao and A-pao plants, respectively) or downregulating S-adenosyl-l-methionine decarboxylase (samdc plants)”

✓ located verbatim in the source · abstract, characters 234–491 · show in text ↑
e1

“A-pao plants accumulated less H2O2 and exhibited less programmed cell death (PCD) than did wild-type plants, in contrast with S-pao and samdc downregulating plants”

✓ located verbatim in the source · abstract, characters 625–788 · show in text ↑
e2

“Upon salt stress, plants secreted spermidine (Spd) into the apoplast, where it was oxidized by the apoplastic PAO, generating H2O2”

✓ located verbatim in the source · abstract, characters 493–623 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

A-pao tobacco plants showed less programmed cell death than wild-type plants under salt stress.

Material
A-pao plantse1
Treatment
salt stresse2
Outcome
programmed cell deathe1
Direction
lesse1
Comparator
wild-type plantse1

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

“we developed a series of tobacco (Nicotiana tabacum cv Xanthi) transgenic plants overexpressing or downregulating apoplastic polyamine oxidase (PAO; S-pao and A-pao plants, respectively) or downregulating S-adenosyl-l-methionine decarboxylase (samdc plants)”

✓ located verbatim in the source · abstract, characters 234–491 · show in text ↑
e1

“A-pao plants accumulated less H2O2 and exhibited less programmed cell death (PCD) than did wild-type plants, in contrast with S-pao and samdc downregulating plants”

✓ located verbatim in the source · abstract, characters 625–788 · show in text ↑
e2

“Upon salt stress, plants secreted spermidine (Spd) into the apoplast, where it was oxidized by the apoplastic PAO, generating H2O2”

✓ located verbatim in the source · abstract, characters 493–623 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

S-pao tobacco plants had higher H2O2 levels under salt stress.

Material
S-pao plantse3
Treatment
salt stresse2
Outcome
H2O2 levelse3
Direction
highere3

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

“we developed a series of tobacco (Nicotiana tabacum cv Xanthi) transgenic plants overexpressing or downregulating apoplastic polyamine oxidase (PAO; S-pao and A-pao plants, respectively) or downregulating S-adenosyl-l-methionine decarboxylase (samdc plants)”

✓ located verbatim in the source · abstract, characters 234–491 · show in text ↑
e2

“Upon salt stress, plants secreted spermidine (Spd) into the apoplast, where it was oxidized by the apoplastic PAO, generating H2O2”

✓ located verbatim in the source · abstract, characters 493–623 · show in text ↑
e3

“S-pao plants, with higher H2O2 levels, failed to accumulate stress-responsive mRNAs, inducing PCD instead”

✓ located verbatim in the source · abstract, characters 1033–1138 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

S-pao tobacco plants failed to accumulate stress-responsive mRNAs under salt stress.

Material
S-pao plantse3
Treatment
salt stresse2
Outcome
stress-responsive mRNAse3
Direction
failed to accumulatee3

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

“we developed a series of tobacco (Nicotiana tabacum cv Xanthi) transgenic plants overexpressing or downregulating apoplastic polyamine oxidase (PAO; S-pao and A-pao plants, respectively) or downregulating S-adenosyl-l-methionine decarboxylase (samdc plants)”

✓ located verbatim in the source · abstract, characters 234–491 · show in text ↑
e2

“Upon salt stress, plants secreted spermidine (Spd) into the apoplast, where it was oxidized by the apoplastic PAO, generating H2O2”

✓ located verbatim in the source · abstract, characters 493–623 · show in text ↑
e3

“S-pao plants, with higher H2O2 levels, failed to accumulate stress-responsive mRNAs, inducing PCD instead”

✓ located verbatim in the source · abstract, characters 1033–1138 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Stress-responsive genes were efficiently induced in wild-type and A-pao plants, at a lower rate in A-pao plants.

Material
wild-type and A-pao plantse4
Treatment
salt stresse2
Outcome
stress-responsive genese4
Direction
efficiently inducede4
Qualifier
at a lower ratee4

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

“we developed a series of tobacco (Nicotiana tabacum cv Xanthi) transgenic plants overexpressing or downregulating apoplastic polyamine oxidase (PAO; S-pao and A-pao plants, respectively) or downregulating S-adenosyl-l-methionine decarboxylase (samdc plants)”

✓ located verbatim in the source · abstract, characters 234–491 · show in text ↑
e2

“Upon salt stress, plants secreted spermidine (Spd) into the apoplast, where it was oxidized by the apoplastic PAO, generating H2O2”

✓ located verbatim in the source · abstract, characters 493–623 · show in text ↑
e4

“in wild-type and A-pao plants, stress-responsive genes were efficiently induced, although in the latter at a lower rate”

✓ located verbatim in the source · abstract, characters 906–1025 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Decreasing intracellular polyamines in samdc downregulating plants enhanced salinity-induced PCD.

Material
samdc downregulating transgenic plantse5
Treatment
decreasing intracellular PAse5
Outcome
salinity-induced PCDe5
Direction
enhancede5

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

“we developed a series of tobacco (Nicotiana tabacum cv Xanthi) transgenic plants overexpressing or downregulating apoplastic polyamine oxidase (PAO; S-pao and A-pao plants, respectively) or downregulating S-adenosyl-l-methionine decarboxylase (samdc plants)”

✓ located verbatim in the source · abstract, characters 234–491 · show in text ↑
e5

“decreasing intracellular PAs, while keeping normal apoplastic Spd oxidation, as in samdc downregulating transgenic plants, caused enhanced salinity-induced PCD”

✓ located verbatim in the source · abstract, characters 1153–1312 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Tobacco plants secreted spermidine into the apoplast under salt stress.

Treatment
salt stresse2
Outcome
secreted spermidinee2
Qualifier
into the apoplaste2

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

“we developed a series of tobacco (Nicotiana tabacum cv Xanthi) transgenic plants overexpressing or downregulating apoplastic polyamine oxidase (PAO; S-pao and A-pao plants, respectively) or downregulating S-adenosyl-l-methionine decarboxylase (samdc plants)”

✓ located verbatim in the source · abstract, characters 234–491 · show in text ↑
e2

“Upon salt stress, plants secreted spermidine (Spd) into the apoplast, where it was oxidized by the apoplastic PAO, generating H2O2”

✓ located verbatim in the source · abstract, characters 493–623 · show in text ↑
Mechanismobservedoriginal resultmeasured

Claim · model-written summary

Apoplastic spermidine oxidized by the apoplastic PAO generates H2O2.

Gene
apoplastic PAOe2
Compound
spermidinee2
Outcome
H2O2e2

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

“we developed a series of tobacco (Nicotiana tabacum cv Xanthi) transgenic plants overexpressing or downregulating apoplastic polyamine oxidase (PAO; S-pao and A-pao plants, respectively) or downregulating S-adenosyl-l-methionine decarboxylase (samdc plants)”

✓ located verbatim in the source · abstract, characters 234–491 · show in text ↑
e2

“Upon salt stress, plants secreted spermidine (Spd) into the apoplast, where it was oxidized by the apoplastic PAO, generating H2O2”

✓ located verbatim in the source · abstract, characters 493–623 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

Induction of stress-responsive genes or PCD depended on the level of spermidine-derived apoplastic H2O2.

Compound
Spd-derived apoplastic H2O2e6
Outcome
Induction of either stress-responsive genes or PCDe6

Not reportedDirection

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

“we developed a series of tobacco (Nicotiana tabacum cv Xanthi) transgenic plants overexpressing or downregulating apoplastic polyamine oxidase (PAO; S-pao and A-pao plants, respectively) or downregulating S-adenosyl-l-methionine decarboxylase (samdc plants)”

✓ located verbatim in the source · abstract, characters 234–491 · show in text ↑
e6

“Induction of either stress-responsive genes or PCD was dependent on the level of Spd-derived apoplastic H2O2”

✓ located verbatim in the source · abstract, characters 790–898 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

Accumulated H2O2 induces tolerance responses or PCD, depending also on intracellular polyamine levels.

Compound
H2O2e7
Outcome
induction of either tolerance responses or PCDe7
Qualifier
depending also on the levels of intracellular PAse7

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

“we developed a series of tobacco (Nicotiana tabacum cv Xanthi) transgenic plants overexpressing or downregulating apoplastic polyamine oxidase (PAO; S-pao and A-pao plants, respectively) or downregulating S-adenosyl-l-methionine decarboxylase (samdc plants)”

✓ located verbatim in the source · abstract, characters 234–491 · show in text ↑
e7

“The accumulated H2O2 results in the induction of either tolerance responses or PCD, depending also on the levels of intracellular PAs”

✓ located verbatim in the source · abstract, characters 1442–1575 · show in text ↑