Paper · 2024 · BMC Genomics

Comparative proteomics in tall fescue to reveal underlying mechanisms for improving Photosystem II thermotolerance during heat stress memory

Guangyang Wang; Xiulei Wang; Dongli Li; et al.

10
claims
19
verbatim quotes
9
citations
2
research areas
✓
Open access · cc-by

Abstract

BACKGROUND: The escalating impacts of global warming intensify the detrimental effects of heat stress on crop growth and yield. Among the earliest and most vulnerable sites of damage is Photosystem II (PSII). Plants exposed to recurring high temperatures develop heat stress memory, a phenomenon that enables them to retain information from previous stress events to better cope with subsequent one. Understanding the components and regulatory networks associated with heat stress memory is crucial for the development of heat-resistant crops. RESULTS: Physiological assays revealed that heat priming (HP) enabled tall fescue to possess higher Photosystem II photochemical activity when subjected to trigger stress. To investigate the underlying mechanisms of heat stress memory, we performed comparative proteomic analyses on tall fescue leaves at S0 (control), R4 (primed), and S5 (triggering), using an integrated approach of Tandem Mass Tag (TMT) labeling and Liquid Chromatography-Mass Spectrometry. A total of 3,851 proteins were detected, with quantitative information available for 3,835 proteins. Among these, we identified 1,423 differentially abundant proteins (DAPs), including 526 proteins that were classified as Heat Stress Memory Proteins (HSMPs). GO and KEGG enrichment analyses revealed that the HSMPs were primarily associated with the "autophagy" in R4 and with "PSII repair", "HSP binding", and "peptidase activity" in S5. Notably, we identified 7 chloroplast-localized HSMPs (HSP21, DJC77, EGY3, LHCA4, LQY1, PSBR and DEGP8, R4/S0 > 1.2, S5/S0 > 1.2), which were considered to be effectors linked to PSII heat stress memory, predominantly in cluster 4. Protein-protein interaction (PPI) analysis indicated that the ubiquitin-proteasome system, with key nodes at UPL3, RAD23b, and UCH3, might play a role in the selective retention of memory effectors in the R4 stage. Furthermore, we conducted RT-qPCR validation on 12 genes, and the results showed that in comparison to the S5 stage, the R4 stage exhibited reduced consistency between transcript and protein levels, providing additional evidence for post-transcriptional regulation in R4. CONCLUSIONS: These findings provide valuable insights into the establishment of heat stress memory under recurring high-temperature episodes and offer a conceptual framework for breeding thermotolerant crops with improved PSII functionality.

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Claims 10

Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Heat priming gave tall fescue higher Photosystem II photochemical activity under trigger stress.

Taxon
tall fescueLolium arundinaceume1
Treatment
heat priming (HP)e1
Outcome
Photosystem II photochemical activitye1
Direction
highere1
Qualifier
when subjected to trigger stresse1

Not reportedComparator

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

Lolium arundinaceum
Lolium arundinaceum · TaxonKrzysztof Ziarnek, Kenraiz · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e1

“Physiological assays revealed that heat priming (HP) enabled tall fescue to possess higher Photosystem II photochemical activity when subjected to trigger stress”

✓ located verbatim in the source · abstract, characters 553–714 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Proteomics identified 1,423 differentially abundant proteins in tall fescue leaves.

Taxon
tall fescueLolium arundinaceume1
Outcome
differentially abundant proteinse3
Value
1,423e3

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

Lolium arundinaceum
Lolium arundinaceum · TaxonKrzysztof Ziarnek, Kenraiz · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e1

“Physiological assays revealed that heat priming (HP) enabled tall fescue to possess higher Photosystem II photochemical activity when subjected to trigger stress”

✓ located verbatim in the source · abstract, characters 553–714 · show in text ↑
e3

“Among these, we identified 1,423 differentially abundant proteins (DAPs), including 526 proteins that were classified as Heat Stress Memory Proteins (HSMPs)”

✓ located verbatim in the source · abstract, characters 1106–1262 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Of the proteins, 526 were classified as Heat Stress Memory Proteins.

Taxon
tall fescueLolium arundinaceume1
Outcome
Heat Stress Memory Proteins (HSMPs)e3
Value
526e3

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

Lolium arundinaceum
Lolium arundinaceum · TaxonKrzysztof Ziarnek, Kenraiz · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e1

“Physiological assays revealed that heat priming (HP) enabled tall fescue to possess higher Photosystem II photochemical activity when subjected to trigger stress”

✓ located verbatim in the source · abstract, characters 553–714 · show in text ↑
e3

“Among these, we identified 1,423 differentially abundant proteins (DAPs), including 526 proteins that were classified as Heat Stress Memory Proteins (HSMPs)”

✓ located verbatim in the source · abstract, characters 1106–1262 · show in text ↑
Observationauthor interpretationoriginal resultmeasured

Claim · model-written summary

Seven chloroplast-localized HSMPs were identified as effectors linked to PSII heat stress memory, predominantly in cluster 4.

Taxon
tall fescueLolium arundinaceume1
Organ / stage
chloroplaste4
Gene
HSP21, DJC77, EGY3, LHCA4, LQY1, PSBR and DEGP8e4
Outcome
chloroplast-localized HSMPse4
Value
7e4
Qualifier
predominantly in cluster 4e4

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

Lolium arundinaceum
Lolium arundinaceum · TaxonKrzysztof Ziarnek, Kenraiz · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e1

“Physiological assays revealed that heat priming (HP) enabled tall fescue to possess higher Photosystem II photochemical activity when subjected to trigger stress”

✓ located verbatim in the source · abstract, characters 553–714 · show in text ↑
e4

“we identified 7 chloroplast-localized HSMPs (HSP21, DJC77, EGY3, LHCA4, LQY1, PSBR and DEGP8, R4/S0 > 1.2, S5/S0 > 1.2), which were considered to be effectors linked to PSII heat stress memory, predominantly in cluster 4”

✓ located verbatim in the source · abstract, characters 1453–1673 · show in text ↑
Mechanismhypothesisoriginal resultbasis n/a

Claim · model-written summary

The ubiquitin-proteasome system, with nodes UPL3, RAD23b and UCH3, might retain memory effectors in the R4 stage.

Taxon
tall fescueLolium arundinaceume1
Organ / stage
R4 stagee5
Gene
UPL3, RAD23b, and UCH3e5
Outcome
selective retention of memory effectorse5

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

Lolium arundinaceum
Lolium arundinaceum · TaxonKrzysztof Ziarnek, Kenraiz · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e1

“Physiological assays revealed that heat priming (HP) enabled tall fescue to possess higher Photosystem II photochemical activity when subjected to trigger stress”

✓ located verbatim in the source · abstract, characters 553–714 · show in text ↑
e5

“Protein-protein interaction (PPI) analysis indicated that the ubiquitin-proteasome system, with key nodes at UPL3, RAD23b, and UCH3, might play a role in the selective retention of memory effectors in the R4 stage”

✓ located verbatim in the source · abstract, characters 1675–1888 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

The R4 stage showed reduced consistency between transcript and protein levels compared with the S5 stage.

Taxon
tall fescueLolium arundinaceume1
Organ / stage
R4 stagee6
Outcome
consistency between transcript and protein levelse6
Direction
reducede6
Comparator
S5 stagee6

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

Lolium arundinaceum
Lolium arundinaceum · TaxonKrzysztof Ziarnek, Kenraiz · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e1

“Physiological assays revealed that heat priming (HP) enabled tall fescue to possess higher Photosystem II photochemical activity when subjected to trigger stress”

✓ located verbatim in the source · abstract, characters 553–714 · show in text ↑
e6

“in comparison to the S5 stage, the R4 stage exhibited reduced consistency between transcript and protein levels”

✓ located verbatim in the source · abstract, characters 1976–2087 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

HSMPs were associated with autophagy in the R4 stage.

Taxon
tall fescueLolium arundinaceume1
Organ / stage
R4e7
Outcome
autophagye7

Not reportedDirection

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

Lolium arundinaceum
Lolium arundinaceum · TaxonKrzysztof Ziarnek, Kenraiz · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e1

“Physiological assays revealed that heat priming (HP) enabled tall fescue to possess higher Photosystem II photochemical activity when subjected to trigger stress”

✓ located verbatim in the source · abstract, characters 553–714 · show in text ↑
e7

“the HSMPs were primarily associated with the "autophagy" in R4”

✓ located verbatim in the source · abstract, characters 1310–1372 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

HSMPs were associated with PSII repair in the S5 stage.

Taxon
tall fescueLolium arundinaceume1
Organ / stage
S5e0
Outcome
PSII repaire0

Not reportedDirection

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

Lolium arundinaceum
Lolium arundinaceum · TaxonKrzysztof Ziarnek, Kenraiz · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e1

“Physiological assays revealed that heat priming (HP) enabled tall fescue to possess higher Photosystem II photochemical activity when subjected to trigger stress”

✓ located verbatim in the source · abstract, characters 553–714 · show in text ↑
e0

“and with "PSII repair", "HSP binding", and "peptidase activity" in S5”

✓ located verbatim in the source · abstract, characters 1373–1442 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

HSMPs were associated with HSP binding in the S5 stage.

Taxon
tall fescueLolium arundinaceume1
Organ / stage
S5e0
Outcome
HSP bindinge0

Not reportedDirection

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

Lolium arundinaceum
Lolium arundinaceum · TaxonKrzysztof Ziarnek, Kenraiz · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e1

“Physiological assays revealed that heat priming (HP) enabled tall fescue to possess higher Photosystem II photochemical activity when subjected to trigger stress”

✓ located verbatim in the source · abstract, characters 553–714 · show in text ↑
e0

“and with "PSII repair", "HSP binding", and "peptidase activity" in S5”

✓ located verbatim in the source · abstract, characters 1373–1442 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

HSMPs were associated with peptidase activity in the S5 stage.

Taxon
tall fescueLolium arundinaceume1
Organ / stage
S5e0
Outcome
peptidase activitye0

Not reportedDirection

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

Lolium arundinaceum
Lolium arundinaceum · TaxonKrzysztof Ziarnek, Kenraiz · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e1

“Physiological assays revealed that heat priming (HP) enabled tall fescue to possess higher Photosystem II photochemical activity when subjected to trigger stress”

✓ located verbatim in the source · abstract, characters 553–714 · show in text ↑
e0

“and with "PSII repair", "HSP binding", and "peptidase activity" in S5”

✓ located verbatim in the source · abstract, characters 1373–1442 · show in text ↑

heat · physiology: photosynthesis · Lolium arundinaceum (tall fescue)Positive and negative results

7 papers: 3 positive, 4 negative or no effect

2 papers in the same direction as this paper · 3 in the opposite direction · 1 reporting no difference from an alternative

  1. negative
  2. negative
  3. negative

3 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.