Paper · 2020 · BMC Plant Biology

SMRT and Illumina RNA sequencing reveal novel insights into the heat stress response and crosstalk with leaf senescence in tall fescue

Yiguang Qian; Liwen Cao; Qiang Zhang; et al.

16
claims
29
verbatim quotes
25
citations
2
research areas
✓
Open access · cc-by

Abstract

BACKGROUND: As a cool-season grass species, tall fescue (Festuca arundinacea) is challenged by increasing temperatures. Heat acclimation or activation of leaf senescence, are two main strategies when tall fescue is exposed to heat stress (HS). However, lacking a genome sequence, the complexity of hexaploidy nature, and the short read of second-generation sequencing hinder a comprehensive understanding of the mechanism. This study aims to characterize the molecular mechanism of heat adaptation and heat-induced senescence at transcriptional and post-transcriptional levels. RESULTS: Transcriptome of heat-treated (1 h and 72 h) and senescent leaves of tall fescue were generated by combining single-molecular real-time and Illumina sequencing. In total, 4076; 6917, and 11,918 differentially expressed genes (DEGs) were induced by short- and long-term heat stress (HS), and senescence, respectively. Venn and bioinformatics analyses of DEGs showed that short-term HS strongly activated heat shock proteins (Hsps) and heat shock factors (Hsfs), as well as specifically activated FK506-binding proteins (FKBPs), calcium signaling genes, glutathione S-transferase genes, photosynthesis-related genes, and phytohormone signaling genes. By contrast, long-term HS shared most of DEGs with senescence, including the up-regulated chlorophyll catabolic genes, phytohormone synthesis/degradation genes, stress-related genes, and NACs, and the down-regulated photosynthesis-related genes, FKBPs, and catalases. Subsequently, transient overexpression in tobacco showed that FaHsfA2a (up-regulated specifically by short-term HS) reduced cell membrane damages caused by HS, but FaNAC029 and FaNAM-B1 (up-regulated by long-term HS and senescence) increased the damages. Besides, alternative splicing was widely observed in HS and senescence responsive genes, including Hsps, Hsfs, and phytohormone signaling/synthesis genes. CONCLUSIONS: The short-term HS can stimulate gene responses and improve thermotolerance, but long-term HS is a damage and may accelerate leaf senescence. These results contribute to our understanding of the molecular mechanism underlying heat adaptation and heat-induced senescence.

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Claims 16

Observationobservedoriginal resultmeasured

Claim · model-written summary

Short-term heat stress induced 4076 differentially expressed genes in tall fescue leaves.

Taxon
tall fescueLolium arundinaceumt0
Outcome
differentially expressed genes (DEGs)e0
Value
4076e0

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

e0

“4076; 6917, and 11,918 differentially expressed genes (DEGs) were induced by short- and long-term heat stress (HS), and senescence, respectively”

✓ located verbatim in the source · abstract, characters 758–902 · show in text ↑
t0

“tall fescue”

✓ located verbatim in the source · title, characters 123–134 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Long-term heat stress induced 6917 differentially expressed genes in tall fescue leaves.

Taxon
tall fescueLolium arundinaceumt0
Outcome
differentially expressed genes (DEGs)e0
Value
6917e0

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

e0

“4076; 6917, and 11,918 differentially expressed genes (DEGs) were induced by short- and long-term heat stress (HS), and senescence, respectively”

✓ located verbatim in the source · abstract, characters 758–902 · show in text ↑
t0

“tall fescue”

✓ located verbatim in the source · title, characters 123–134 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Leaf senescence involved 11,918 differentially expressed genes in tall fescue.

Taxon
tall fescueLolium arundinaceumt0
Outcome
differentially expressed genes (DEGs)e0
Value
11,918e0

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

e0

“4076; 6917, and 11,918 differentially expressed genes (DEGs) were induced by short- and long-term heat stress (HS), and senescence, respectively”

✓ located verbatim in the source · abstract, characters 758–902 · show in text ↑
t0

“tall fescue”

✓ located verbatim in the source · title, characters 123–134 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Short-term heat stress strongly activated heat shock proteins and heat shock factors in tall fescue.

Taxon
tall fescueLolium arundinaceumt0
Outcome
heat shock proteins (Hsps) and heat shock factors (Hsfs)e0
Direction
activatede0
Qualifier
short-term HSe0

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

e0

“short-term HS strongly activated heat shock proteins (Hsps) and heat shock factors (Hsfs), as well as specifically activated FK506-binding proteins (FKBPs), calcium signaling genes, glutathione S-transferase genes, photosynthesis-related genes, and phytohormone signaling genes”

✓ located verbatim in the source · abstract, characters 957–1234 · show in text ↑
t0

“tall fescue”

✓ located verbatim in the source · title, characters 123–134 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Short-term heat stress specifically activated FKBPs, calcium signaling genes and glutathione S-transferase genes in tall fescue.

Taxon
tall fescueLolium arundinaceumt0
Outcome
FK506-binding proteins (FKBPs), calcium signaling genes, glutathione S-transferase genese0
Direction
activatede0
Qualifier
short-term HSe0

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

e0

“short-term HS strongly activated heat shock proteins (Hsps) and heat shock factors (Hsfs), as well as specifically activated FK506-binding proteins (FKBPs), calcium signaling genes, glutathione S-transferase genes, photosynthesis-related genes, and phytohormone signaling genes”

✓ located verbatim in the source · abstract, characters 957–1234 · show in text ↑
t0

“tall fescue”

✓ located verbatim in the source · title, characters 123–134 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Short-term heat stress specifically activated photosynthesis-related genes and phytohormone signaling genes in tall fescue.

Taxon
tall fescueLolium arundinaceumt0
Outcome
photosynthesis-related genes, and phytohormone signaling genese0
Direction
activatede0
Qualifier
short-term HSe0

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

e0

“short-term HS strongly activated heat shock proteins (Hsps) and heat shock factors (Hsfs), as well as specifically activated FK506-binding proteins (FKBPs), calcium signaling genes, glutathione S-transferase genes, photosynthesis-related genes, and phytohormone signaling genes”

✓ located verbatim in the source · abstract, characters 957–1234 · show in text ↑
t0

“tall fescue”

✓ located verbatim in the source · title, characters 123–134 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Long-term heat stress shared most of its differentially expressed genes with senescence in tall fescue.

Taxon
tall fescueLolium arundinaceumt0
Outcome
shared most of DEGs with senescencee0
Qualifier
long-term HSe0

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

e0

“long-term HS shared most of DEGs with senescence, including the up-regulated chlorophyll catabolic genes, phytohormone synthesis/degradation genes, stress-related genes, and NACs, and the down-regulated photosynthesis-related genes, FKBPs, and catalases”

✓ located verbatim in the source · abstract, characters 1249–1502 · show in text ↑
t0

“tall fescue”

✓ located verbatim in the source · title, characters 123–134 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Long-term heat stress and senescence shared up-regulated chlorophyll catabolic genes, phytohormone synthesis/degradation genes and stress-related genes.

Taxon
tall fescueLolium arundinaceumt0
Outcome
chlorophyll catabolic genes, phytohormone synthesis/degradation genes, stress-related genese0
Direction
up-regulatede0
Qualifier
long-term HSe0

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

e0

“long-term HS shared most of DEGs with senescence, including the up-regulated chlorophyll catabolic genes, phytohormone synthesis/degradation genes, stress-related genes, and NACs, and the down-regulated photosynthesis-related genes, FKBPs, and catalases”

✓ located verbatim in the source · abstract, characters 1249–1502 · show in text ↑
t0

“tall fescue”

✓ located verbatim in the source · title, characters 123–134 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Long-term heat stress and senescence shared up-regulated NAC genes in tall fescue.

Taxon
tall fescueLolium arundinaceumt0
Outcome
NACse0
Direction
up-regulatede0
Qualifier
long-term HSe0

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

e0

“long-term HS shared most of DEGs with senescence, including the up-regulated chlorophyll catabolic genes, phytohormone synthesis/degradation genes, stress-related genes, and NACs, and the down-regulated photosynthesis-related genes, FKBPs, and catalases”

✓ located verbatim in the source · abstract, characters 1249–1502 · show in text ↑
t0

“tall fescue”

✓ located verbatim in the source · title, characters 123–134 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Long-term heat stress and senescence shared down-regulated photosynthesis-related genes, FKBPs and catalases.

Taxon
tall fescueLolium arundinaceumt0
Outcome
photosynthesis-related genes, FKBPs, and catalasese0
Direction
down-regulatede0
Qualifier
long-term HSe0

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

e0

“long-term HS shared most of DEGs with senescence, including the up-regulated chlorophyll catabolic genes, phytohormone synthesis/degradation genes, stress-related genes, and NACs, and the down-regulated photosynthesis-related genes, FKBPs, and catalases”

✓ located verbatim in the source · abstract, characters 1249–1502 · show in text ↑
t0

“tall fescue”

✓ located verbatim in the source · title, characters 123–134 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Transient overexpression of FaHsfA2a in tobacco reduced cell membrane damage caused by heat stress.

Treatment
transient overexpressione0
Gene
FaHsfA2ae0
Outcome
cell membrane damages caused by HSe0
Direction
reducede0

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

“transient overexpression in tobacco showed that FaHsfA2a (up-regulated specifically by short-term HS) reduced cell membrane damages caused by HS, but FaNAC029 and FaNAM-B1 (up-regulated by long-term HS and senescence) increased the damages”

✓ located verbatim in the source · abstract, characters 1518–1757 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Transient overexpression of FaNAC029 in tobacco increased cell membrane damage caused by heat stress.

Treatment
transient overexpressione0
Gene
FaNAC029e0
Outcome
damagese0
Direction
increasede0

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

“transient overexpression in tobacco showed that FaHsfA2a (up-regulated specifically by short-term HS) reduced cell membrane damages caused by HS, but FaNAC029 and FaNAM-B1 (up-regulated by long-term HS and senescence) increased the damages”

✓ located verbatim in the source · abstract, characters 1518–1757 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Transient overexpression of FaNAM-B1 in tobacco increased cell membrane damage caused by heat stress.

Treatment
transient overexpressione0
Gene
FaNAM-B1e0
Outcome
damagese0
Direction
increasede0

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

“transient overexpression in tobacco showed that FaHsfA2a (up-regulated specifically by short-term HS) reduced cell membrane damages caused by HS, but FaNAC029 and FaNAM-B1 (up-regulated by long-term HS and senescence) increased the damages”

✓ located verbatim in the source · abstract, characters 1518–1757 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Alternative splicing was widely observed in heat stress and senescence responsive genes of tall fescue, including Hsps, Hsfs and phytohormone signaling/synthesis genes.

Taxon
tall fescueLolium arundinaceumt0
Outcome
alternative splicinge0
Qualifier
widely observede0

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

e0

“alternative splicing was widely observed in HS and senescence responsive genes”

✓ located verbatim in the source · abstract, characters 1768–1846 · show in text ↑
t0

“tall fescue”

✓ located verbatim in the source · title, characters 123–134 · show in text ↑
Intervention effectauthor interpretationoriginal resultpositivemeasured

Claim · model-written summary

The authors conclude that short-term heat stress can stimulate gene responses and improve thermotolerance in tall fescue.

Taxon
tall fescueLolium arundinaceumt0
Treatment
short-term HSe0
Outcome
thermotolerancee0
Direction
improvee0

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

e0

“The short-term HS can stimulate gene responses and improve thermotolerance, but long-term HS is a damage and may accelerate leaf senescence”

✓ located verbatim in the source · abstract, characters 1927–2066 · show in text ↑
t0

“tall fescue”

✓ located verbatim in the source · title, characters 123–134 · show in text ↑
Intervention effectauthor interpretationoriginal resultnegativemeasured

Claim · model-written summary

The authors conclude that long-term heat stress is damaging and may accelerate leaf senescence in tall fescue.

Taxon
tall fescueLolium arundinaceumt0
Treatment
long-term HSe0
Outcome
leaf senescencee0
Direction
acceleratee0

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

e0

“The short-term HS can stimulate gene responses and improve thermotolerance, but long-term HS is a damage and may accelerate leaf senescence”

✓ located verbatim in the source · abstract, characters 1927–2066 · show in text ↑
t0

“tall fescue”

✓ located verbatim in the source · title, characters 123–134 · show in text ↑

heat · tolerance: abiotic · Lolium arundinaceum (tall fescue)Results agree

2 papers: 2 positive, 0 negative or no effect

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