Paper · 2024 · Journal of Biological Chemistry

In-depth analysis of isochorismate synthase-derived metabolism in plant immunity: Identification of meta-substituted benzoates and salicyloyl-malate

Nicola Scholten; Michael Hartmann; Sarah Abts; et al.

16
claims
30
verbatim quotes
5
citations
3
research areas
✓
Open access · cc-by

Abstract

Isochorismate-derived metabolism enables biosynthesis of the plant defense hormone salicylic acid (SA) and its derivatives. In Arabidopsis thaliana, the stress-induced accumulation of SA depends on ISOCHORISMATE SYNTHASE1 (ICS1) and also requires the presumed isochorismate transporter ENHANCED DISEASE SUSCEPTIBILITY5 (EDS5) and the GH3 enzyme avrPphB SUSCEPTIBLE3 (PBS3). By comparative metabolite and structural analyses, we identified several hitherto unreported ICS1- and EDS5-dependent, biotic stress-inducible Arabidopsis metabolites. These involve meta-substituted SA derivatives (5-formyl-SA, 5-carboxy-SA, 5-carboxymethyl-SA), their benzoic acid (BA) analogs (3-formyl-BA, 3-carboxy-BA, 3-carboxymethyl-BA), and besides the previously detected salicyloyl-aspartate (SA-Asp), the ester conjugate salicyloyl-malate (SA-Mal). SA functions as a biosynthetic precursor for SA-Mal and SA-Asp, but not for the meta-substituted SA- and BA-derivatives, which accumulate to moderate levels at later stages of bacterial infection. Interestingly, Arabidopsis leaves possess oxidizing activity to effectively convert meta-formyl- into meta-carboxy-SA/BAs. In contrast to SA, exogenously applied meta-substituted SA/BA-derivatives and SA-Mal exert a moderate impact on plant immunity and defence-related gene expression. While the isochorismate-derived metabolites are negatively regulated by the SA receptor NON-EXPRESSOR OF PR GENES1, SA conjugates (SA-Mal, SA-Asp, SA-glucose conjugates) and meta-substituted SA/BA-derivatives are oppositely affected by PBS3. Notably, our data indicate a PBS3-independent path to isochorismate-derived SA at later stages of bacterial infection, which does not considerably impact immune-related characteristics. Moreover, our results argue against a previously proposed role of EDS5 in the biosynthesis of the immune signal N-hydroxypipecolic acid and associated transport processes. We propose a significantly extended biochemical scheme of plant isochorismate metabolism that involves an alternative generation mode for benzoate- and salicylate-derivatives.

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Claims 16

Observationobservedoriginal resultmeasured

Claim · model-written summary

Several previously unreported ICS1- and EDS5-dependent Arabidopsis metabolites were identified.

Taxon
ArabidopsisArabidopsise0
Gene
ICS1- and EDS5-dependente0
Outcome
biotic stress-inducible Arabidopsis metabolitese0

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

Arabidopsis
Arabidopsis · Taxon · picture of the genus (one of its species)Original uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“we identified several hitherto unreported ICS1- and EDS5-dependent, biotic stress-inducible Arabidopsis metabolites”

✓ located verbatim in the source · abstract, characters 425–540 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

The identified metabolites included meta-substituted salicylic acid derivatives.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Outcome
meta-substituted SA derivatives (5-formyl-SA, 5-carboxy-SA, 5-carboxymethyl-SA)e0

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“meta-substituted SA derivatives (5-formyl-SA, 5-carboxy-SA, 5-carboxymethyl-SA)”

✓ located verbatim in the source · abstract, characters 556–635 · show in text ↑
t0

“In Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 124–147 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

The identified metabolites included three benzoic acid analogs.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Outcome
benzoic acid (BA) analogs (3-formyl-BA, 3-carboxy-BA, 3-carboxymethyl-BA)e0

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“their benzoic acid (BA) analogs (3-formyl-BA, 3-carboxy-BA, 3-carboxymethyl-BA)”

✓ located verbatim in the source · abstract, characters 637–716 · show in text ↑
t0

“In Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 124–147 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Salicyloyl-malate was identified as an ester conjugate.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Outcome
ester conjugate salicyloyl-malate (SA-Mal)e0

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“the ester conjugate salicyloyl-malate (SA-Mal)”

✓ located verbatim in the source · abstract, characters 785–831 · show in text ↑
t0

“In Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 124–147 · show in text ↑
Mechanismobservedoriginal resultmeasured

Claim · model-written summary

Salicylic acid was a biosynthetic precursor for SA-Mal and SA-Asp.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Compound
SAe0
Outcome
SA-Mal and SA-Aspe0

Not reportedDirection

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“SA functions as a biosynthetic precursor for SA-Mal and SA-Asp”

✓ located verbatim in the source · abstract, characters 833–895 · show in text ↑
t0

“In Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 124–147 · show in text ↑
Mechanismobservedoriginal resultmeasured

Claim · model-written summary

Salicylic acid was not a precursor for the meta-substituted SA and BA derivatives.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Compound
SAe0
Outcome
meta-substituted SA- and BA-derivativese0

Not reportedDirection

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“SA functions as a biosynthetic precursor for SA-Mal and SA-Asp, but not for the meta-substituted SA- and BA-derivatives”

✓ located verbatim in the source · abstract, characters 833–952 · show in text ↑
t0

“In Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 124–147 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Meta-substituted SA and BA derivatives accumulated moderately at later bacterial infection stages.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Outcome
meta-substituted SA- and BA-derivativese0
Direction
accumulatee0
Qualifier
later stages of bacterial infectione0

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“meta-substituted SA- and BA-derivatives, which accumulate to moderate levels at later stages of bacterial infection”

✓ located verbatim in the source · abstract, characters 913–1028 · show in text ↑
t0

“In Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 124–147 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Arabidopsis leaves converted meta-formyl derivatives into meta-carboxy SA and BA derivatives.

Taxon
ArabidopsisArabidopsise0
Organ / stage
leavese0
Outcome
oxidizing activitye0
Qualifier
convert meta-formyl- into meta-carboxy-SA/BAse0

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

Arabidopsis
Arabidopsis · Taxon · picture of the genus (one of its species)Original uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“Arabidopsis leaves possess oxidizing activity to effectively convert meta-formyl- into meta-carboxy-SA/BAs”

✓ located verbatim in the source · abstract, characters 1045–1151 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Applied meta-substituted derivatives and SA-Mal moderately affected immunity.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Treatment
exogenously applied meta-substituted SA/BA-derivatives and SA-Male0
Outcome
plant immunitye0

Not reportedComparatorDirection

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“exogenously applied meta-substituted SA/BA-derivatives and SA-Mal exert a moderate impact on plant immunity”

✓ located verbatim in the source · abstract, characters 1172–1279 · show in text ↑
t0

“In Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 124–147 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Applied meta-substituted derivatives and SA-Mal moderately affected defence gene expression.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Treatment
exogenously applied meta-substituted SA/BA-derivatives and SA-Male0
Outcome
defence-related gene expressione0

Not reportedComparatorDirection

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“exogenously applied meta-substituted SA/BA-derivatives and SA-Mal exert a moderate impact on plant immunity and defence-related gene expression”

✓ located verbatim in the source · abstract, characters 1172–1315 · show in text ↑
t0

“In Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 124–147 · show in text ↑
Mechanismobservedoriginal resultmeasured

Claim · model-written summary

NON-EXPRESSOR OF PR GENES1 negatively regulated isochorismate-derived metabolites.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Gene
NON-EXPRESSOR OF PR GENES1e0
Outcome
isochorismate-derived metabolitese0
Direction
negatively regulatede0

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“the isochorismate-derived metabolites are negatively regulated by the SA receptor NON-EXPRESSOR OF PR GENES1”

✓ located verbatim in the source · abstract, characters 1323–1431 · show in text ↑
t0

“In Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 124–147 · show in text ↑
Mechanismobservedoriginal resultmeasured

Claim · model-written summary

PBS3 affected SA conjugates and meta-substituted derivatives in opposite directions.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Gene
PBS3e0
Outcome
SA conjugates (SA-Mal, SA-Asp, SA-glucose conjugates) and meta-substituted SA/BA-derivativese0
Direction
oppositely affectede0

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“SA conjugates (SA-Mal, SA-Asp, SA-glucose conjugates) and meta-substituted SA/BA-derivatives are oppositely affected by PBS3”

✓ located verbatim in the source · abstract, characters 1433–1557 · show in text ↑
t0

“In Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 124–147 · show in text ↑
Mechanismobservedoriginal resultmeasured

Claim · model-written summary

A PBS3-independent route to isochorismate-derived SA operated late in bacterial infection.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Gene
PBS3e0
Outcome
isochorismate-derived SAe0
Qualifier
later stages of bacterial infectione0

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“a PBS3-independent path to isochorismate-derived SA at later stages of bacterial infection”

✓ located verbatim in the source · abstract, characters 1586–1676 · show in text ↑
t0

“In Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 124–147 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

That route had little impact on immune-related characteristics.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Outcome
immune-related characteristicse0
Direction
does not considerably impacte0

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“which does not considerably impact immune-related characteristics”

✓ located verbatim in the source · abstract, characters 1678–1743 · show in text ↑
t0

“In Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 124–147 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

Results argued against an EDS5 role in N-hydroxypipecolic acid biosynthesis and transport.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Gene
EDS5e0
Outcome
biosynthesis of the immune signal N-hydroxypipecolic acid and associated transport processese0

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“our results argue against a previously proposed role of EDS5 in the biosynthesis of the immune signal N-hydroxypipecolic acid and associated transport processes”

✓ located verbatim in the source · abstract, characters 1755–1915 · show in text ↑
t0

“In Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 124–147 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

The authors proposed an extended isochorismate scheme with another route to benzoate and salicylate derivatives.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Outcome
benzoate- and salicylate-derivativese0
Qualifier
alternative generation modee0

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

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“We propose a significantly extended biochemical scheme of plant isochorismate metabolism that involves an alternative generation mode for benzoate- and salicylate-derivatives”

✓ located verbatim in the source · abstract, characters 1917–2091 · show in text ↑
t0

“In Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 124–147 · show in text ↑