Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2016 Jan 11:6:1226.
doi: 10.3389/fpls.2015.01226. eCollection 2015.

Heat Shock Factor Genes of Tall Fescue and Perennial Ryegrass in Response to Temperature Stress by RNA-Seq Analysis

Yan Wang  1 , Ya Dai  2 , Xiang Tao  1 , Jia-Zhen Wang  3 , Hai-Yang Cheng  1 , Hong Yang  1 , Xin-Rong Ma  1
Affiliations

Heat Shock Factor Genes of Tall Fescue and Perennial Ryegrass in Response to Temperature Stress by RNA-Seq Analysis

Yan Wang et al. Front Plant Sci. .

Abstract

Heat shock factors (Hsfs) are important regulators of stress-response in plants. However, our understanding of Hsf genes and their responses to temperature stresses in two Pooideae cool-season grasses, Festuca arundinacea, and Lolium perenne, is limited. Here we conducted comparative transcriptome analyses of plant leaves exposed to heat or cold stress for 10 h. Approximately, 30% and 25% of the genes expressed in the two species showed significant changes under heat and cold stress, respectively, including subsets of Hsfs and their target genes. We uncovered 74 Hsfs in F. arundinacea and 52 Hsfs in L. perenne, and categorized these genes into three subfamilies, HsfA, HsfB, and HsfC based on protein sequence homology to known Hsf members in model organisms. The Hsfs showed a strong response to heat and/or cold stress. The expression of HsfAs was elevated under heat stress, especially in class HsfA2, which exhibited the most dramatic responses. HsfBs were upregulated by the both temperature conditions, and HsfCs mainly showed an increase in expression under cold stress. The target genes of Hsfs, such as heat shock protein (HSP), ascorbate peroxidase (APX), inositol-3-phosphate synthase (IPS), and galactinol synthase (GOLS1), showed strong and unique responses to different stressors. We comprehensively detected Hsfs and their target genes in F. arundinacea and L. perenne, providing a foundation for future gene function studies and genetic engineering to improve stress tolerance in grasses and other crops.

Keywords: RNA-Seq; cold stress; expression analysis; heat shock factors (Hsfs); heat stress; perennial ryegrass; phylogenetic analysis; tall fescue.

PubMed Disclaimer

Figures

Figure 1
Figure 1
Analysis of differentially expressed genes (DEGs) in tall fescue and perennial ryegrass transcriptomes in response to heat and cold stress. (A) Up- and down-regulated DEGs under heat or cold stress in the two grass species. Up (red) indicates upregulated DEGs, and down (blue) represents downregulated DEGs. (B) Shared and divergent DEGs in the tall fescue or perennial ryegrass under heat and cold stress. Heat-up (red) indicates the upregulated DEGs under heat stress; heat-down (green) represents the downregulated DEGs under heat stress; cold-up (blue) denotes the upregulated DEGs under cold stress; and cold-down (yellow) represents the downregulated DEGs under cold stress.
Figure 2
Figure 2
Neighbor–joining phylogenetic tree of Hsf proteins from the tall fescue, perennial ryegrass, Brachypodium distachyon, and Arabidopsis thaliana. Hsfs in Brachypodium distachyon are prefixed by Bd, and Hsfs in Arabidopsis thaliana are prefixed by At. Hsfs in tall fescue are marked by a “Fa” prefix and sequence-ID in the transcriptome. Hsfs in perennial ryegrass are marked by a “Lp” prefix and a sequence-ID in the transcriptome.
Figure 3
Figure 3
Heatmaps of the expression profiles of Hsf genes in the two grass species subjected to heat and cold stress. Heat-log2 Ratio indicates the fold-change of Hsf FPKM values under HS, and cold-log2 Ratio represents the fold-change of Hsf FPKM values under CS. The black grid denotes genes where we did not detect expression.
Figure 4
Figure 4
The expression patterns of heat shock factors in the tall fescue and perennial ryegrass under heat and cold stress. Slight-up (pink) indicates insignificantly upregulated Hsf genes, sig-up (red) represents significantly upregulated Hsf genes, slight-down (light blue) denotes insignificantly downregulated Hsf genes, and sig-down (blue) denotes significantly downregulated Hsf genes. Significant differences in transcript expression levels were determined by setting the thresholds for false discovery rate as “(FDR) < 0.001” and “|log2 Ratio| ≥ 1,” where ratio indicates the fold-change of FPKM values for the treatment and control samples.
Figure 5
Figure 5
Stress-response analyses of different Hsf classes showing significant expression differences at least one stress condition. “Up-HS only” indicates upregulated heat shock factors (Hsfs) only under heat stress (HS); “Down-HS only” represents downregulated Hsfs only under HS; “Up-CS only” represents upregulated Hsfs only under cold stress (CS); and “Down-CS only” denotes downregulated Hsfs only under CS. “Com up-HS and CS” indicates upregulated Hsfs under HS and CS, and “Com down-HS and CS” represents downregulated Hsfs under HS and CS. “Up-HS and Down-CS” shows Hsfs upregulated under HS and downregulated under CS, and “Up-CS and Down-HS” denotes Hsfs downregualted under HS and upregulated under CS.
Figure 6
Figure 6
Venn diagram of differentially expressed target genes of Hsfs in the tall fescue or perennial ryegrass under heat and cold temperature stress. Red (heat-up) represents the upregulated target transcripts under heat stress; green (heat-down) represents the downregulated target transcripts under heat stress; blue (cold-up) indicates the upregulated target transcripts under cold stress; and yellow (cold-down) represents the down-regulated target transcripts under cold stress.
Figure 7
Figure 7
Overall expression differences (log2 Ratio) of heat shock factors and their target genes between species and stresses. (A) Heat shock factor genes. (B) The target genes of heat shock factors. Abbreviations are as follows: Fa, tall fescue (Festuca arundinacea); Lp, perennial ryegrass (Lolium perenne); HS, heat stress; and CS, cold stress. The log2 Ratio represents the fold-change of Hsf FPKM values under heat or cold treatment relative to that of the control samples.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Almoguera C., Rojas A., Díaz-Martín J., Prieto-Dapena P., Carranco R., Jordano J. (2002). A seed-specific heat-shock transcription factor involved in developmental regulation during embryogenesis in sunflower. J. Biol. Chem. 277, 43866–43872. 10.1074/jbc.M207330200 - DOI - PubMed
    1. Audic S., Claverie J. M. (1997). The significance of digital gene expression profiles. Genome Res. 7, 986–995. 10.1101/gr.7.10.986 - DOI - PubMed
    1. Baniwal S. K., Chan K. Y., Scharf K. D., Nover L. (2007). Role of heat stress transcription factor HsfA5 as specific repressor of HsfA4. J. Biol. Chem. 282, 3605–3613. 10.1074/jbc.M609545200 - DOI - PubMed
    1. Bharti K., von Koskull-Döring P., Bharti S., Kumar P., Tintschl-Körbitzer A., Treuter E., et al. . (2004). Tomato heat stress transcription factor HsfB1 represents a novel type of general transcription coactivator with a histone-like motif interacting with the plant CREB binding protein ortholog HAC1. Plant Cell 16, 1521–1535. 10.1105/tpc.019927 - DOI - PMC - PubMed
    1. Carranco R., Espinosa J. M., Prieto-Dapena P., Almoguera C., Jordano J. (2010). Repression by an auxin/indole acetic acid protein connects auxin signaling with heat shock factor-mediated seed longevity. Proc. Natl. Acad. Sci. U.S.A. 107, 21908–21913. 10.1073/pnas.1014856107 - DOI - PMC - PubMed

LinkOut - more resources