Paper · 2023 · Plant Communications

Alternaria TeA toxin activates a chloroplast retrograde signaling pathway to facilitate JA-dependent pathogenicity

Jiale Shi; He Wang; Mengping Li; et al.

6
claims
11
verbatim quotes
20
citations
3
research areas
✓
Open access · cc-by-nc-nd

Abstract

The chloroplast is a critical battleground in the arms race between plants and pathogens. Among microbe-secreted mycotoxins, the tenuazonic acid (TeA), produced by the genus Alternaria and other phytopathogenic fungi, inhibits photosynthesis, leading to a burst of photosynthetic singlet oxygen (1O2) implicated in damage and chloroplast-to-nucleus retrograde signaling. Despite the potent adversity of Alternaria pathogens on crop production, the molecular mechanism of TeA-caused pathogenicity and cognate plant defense responses remain fragmented. We now reveal that A. alternata induces necrotrophic foliar lesions by harnessing an EXECUTER1 (EX1)/EX2-mediated chloroplast-to-nucleus retrograde signaling (RS), activated by TeA toxin-derived photosynthetic 1O2 in Arabidopsis thaliana. Mutation of 1O2-sensitive EX1-W643 or complete deletion of the SOS (Singlet Oxygen Sensor) domain of EX1 compromises the expression of 1O2-responsive nuclear genes and foliar lesions. Remarkably, we further noticed that the TeA toxin rapidly induces nuclear genes implicated in jasmonic acid (JA) synthesis and signaling, for which EX1-mediated RS appeared to be critical in establishing a signaling cascade from 1O2 to JA. Our present study sheds new light on A. alternata-caused foliar pathogenicity, where EX1-dependent 1O2 signaling induces JA-dependent foliar cell death.

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Claims 6

Mechanismauthor interpretationoriginal resultnegativemeasured

Claim · model-written summary

A. alternata induced necrotrophic foliar lesions through EX1/EX2-mediated chloroplast retrograde signaling.

Taxon
Arabidopsis thalianaArabidopsis thalianae0
Interactor
A. alternataAlternaria alternatae0pathogen
Gene
EXECUTER1 (EX1)/EX2e0
Outcome
necrotrophic foliar lesionse0
Qualifier
chloroplast-to-nucleus retrograde signaling (RS)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 ↗
Alternaria alternata
Alternaria alternata · Interactor · picture from its Wikimedia Commons categoryMarta Hiromi Taniwaki, Secretaria de Agricultura e Abastecimento · CC BY 2.0 · Wikimedia Commons ↗

Verbatim

e0

“A. alternata induces necrotrophic foliar lesions by harnessing an EXECUTER1 (EX1)/EX2-mediated chloroplast-to-nucleus retrograde signaling (RS), activated by TeA toxin-derived photosynthetic 1O2 in Arabidopsis thaliana.”

✓ located verbatim in the source · abstract, characters 570–789 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Mutation of EX1-W643 or deletion of the EX1 SOS domain compromised 1O2-responsive nuclear gene expression.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Treatment
Mutation of 1O2-sensitive EX1-W643 or complete deletion of the SOS (Singlet Oxygen Sensor) domain of EX1e0
Gene
EX1-W643e0
Outcome
expression of 1O2-responsive nuclear genese0
Direction
compromisese0

Not reportedComparator

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

“Mutation of 1O2-sensitive EX1-W643 or complete deletion of the SOS (Singlet Oxygen Sensor) domain of EX1 compromises the expression of 1O2-responsive nuclear genes and foliar lesions.”

✓ located verbatim in the source · abstract, characters 790–973 · show in text ↑
t0

“Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 768–788 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Mutation or SOS-domain deletion in EX1 compromised foliar lesions.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Treatment
Mutation of 1O2-sensitive EX1-W643 or complete deletion of the SOS (Singlet Oxygen Sensor) domain of EX1e0
Gene
EX1-W643e0
Outcome
foliar lesionse0
Direction
compromisese0

Not reportedComparator

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

“Mutation of 1O2-sensitive EX1-W643 or complete deletion of the SOS (Singlet Oxygen Sensor) domain of EX1 compromises the expression of 1O2-responsive nuclear genes and foliar lesions.”

✓ located verbatim in the source · abstract, characters 790–973 · show in text ↑
t0

“Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 768–788 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

TeA rapidly induced nuclear genes involved in jasmonic-acid synthesis and signaling.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Treatment
TeA toxine0
Outcome
nuclear genes implicated in jasmonic acid (JA) synthesis and signalinge0
Direction
inducese0

Not reportedComparator

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 TeA toxin rapidly induces nuclear genes implicated in jasmonic acid (JA) synthesis and signaling”

✓ located verbatim in the source · abstract, characters 1010–1110 · show in text ↑
t0

“Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 768–788 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

EX1-mediated signaling was critical for the signaling cascade from singlet oxygen to JA.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Gene
EX1e0
Outcome
signaling cascade from 1O2 to JAe0
Qualifier
appeared to be criticale0

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

“EX1-mediated RS appeared to be critical in establishing a signaling cascade from 1O2 to JA”

✓ located verbatim in the source · abstract, characters 1122–1212 · show in text ↑
t0

“Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 768–788 · show in text ↑
Mechanismauthor interpretationoriginal resultnegativemeasured

Claim · model-written summary

EX1-dependent singlet-oxygen signaling induced JA-dependent foliar cell death.

Taxon
Arabidopsis thalianaArabidopsis thalianat0
Gene
EX1e0
Outcome
JA-dependent foliar cell deathe0
Qualifier
EX1-dependent 1O2 signalinge0

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

“EX1-dependent 1O2 signaling induces JA-dependent foliar cell death”

✓ located verbatim in the source · abstract, characters 1299–1365 · show in text ↑
t0

“Arabidopsis thaliana”

✓ located verbatim in the source · abstract, characters 768–788 · show in text ↑

loss of function · molecular: expression · Arabidopsis thaliana (thale cress)Positive and negative results

73 papers: 13 positive, 60 negative or no effect

59 papers in the same direction as this paper · 13 in the opposite direction

  1. positive
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loss of function · disease · Arabidopsis thaliana (thale cress)Positive and negative results

82 papers: 31 positive, 51 negative or no effect

30 papers in the same direction as this paper · 51 in the opposite direction

  1. negative
  2. negative
  3. negative

78 papers more in this group

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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.