Integrated transcriptomic, metabolomic and lipidomic analyses uncover the crucial roles of lipid metabolism pathways in oat (Avena sativa) responses to heat stress

Abstract

Background: Oat (Avena sativa), an economically important cereal crop globally, is highly vulnerable to high-temperature stress, challenging its geographic distribution and grain production. However, the mechanisms underlying oat's response to heat stress remain pooly understood.

Results: A time-course transcriptome revealed significant enrichment in lipid metabolism pathways during heat stress, which was corroborated by metabolomic findings. Integrated co-expression network analysis and KEGG enrichment further underscored the critical role of lipid metabolism in oat's adaptive response to heat stress. Comprehensive lipidomic profiling of heat-stressed oat seedlings demonstrated a substantial increase in the proportion of neutral lipids, suggesting an evolutionarily conserved protective strategy. Synergistic transcriptional responses indicated that heat-induced triacylglycerol (TAG) accumulation primarily originated from extensive membrane lipid turnover rather than de novo fatty acid (FA) synthesis, with the Kennedy pathway serving as the dominant route for TAG production. Enhanced phospholipid hydrolysis, acyl editing, and endoplasmic reticulum-localized FA desaturation collectively contributed to TAG enrichment in polyunsaturated FAs. Additionally, elevated levels of phosphatidylglycerol (PG) and phosphatidylinositol (PI) in oat may confer adaptive benefits under heat stress.

Conclusions: This study demonstrates that lipid metabolism critically regulates heat stress response in oat. The findings provide valuable target genes for genetic improvement in enhancing oat thermotolerance.

Keywords: Avena sativa; Heat stress; Lipid metabolism; Lipidome; Metabolome; Transcriptome.

Fig. 1

Transcriptomic response of oat seedlings to heat stress. A PCA score plot of gene expression profiles. B The number of DEGs between different comparison groups. Upregulation is represented by red, and downregulation is represented by blue. C Venn diagram showing the overlap of DEGs detected at each specific time point

Fig. 2

KEGG pathway enrichment of heat-responsive DEGs at 3 h (A), 6 h (B), 9 h (C), and the core DEGs shared across all time points (D)

Fig. 3

KEGG pathway enrichment of DAMs at 3 h (A), 6 h (B), and 9 h (C) after heat treatment

Fig. 4

Correlation analysis of transcriptomic and metabolomic data. A Nine-quadrant diagram of metabolite and gene expression patterns. B The top 10 significantly enriched KEGG pathways of genes and metabolites in the quadrants 3 and 7

Fig. 5

Comprehensive analysis of heat-induced lipidomic alterations in oat seedlings. A Total lipid content in control (CK) and heat-stressed (HS) oat seedlings. B Relative abundance of major lipid classes (as a percentage of total lipids) and the molecular species composition within each class for CK and HS seedlings. C-F Molecular species composition of specific lipid classes in CK and HS seedlings: (C) Phospholipids, (D) Neutral lipids, (E) Glycolipids, (F) Lysophospholipids. Statistically significant differences between CK and HS groups were determined by Student’s t-test (*, P < 0.05; **, P < 0.01)

Fig. 6

Heatmap of the most significantly altered lipid molecular species in oat seedlings under heat stress

Fig. 7

Lipid metabolism and associated gene expression profiles in heat-stressed oat seedling. A Schematic representation of the lipid metabolic network in oat seedlings. B Heatmap visualization of gene expression patterns associated with fatty acid (FA) de novo synthesis, phospholipid and galactolipid metabolism, and triacylglycerol (TAG) assembly. Red and white color gradients denote upregulated and downregulated gene expression, respectively, in oat seedlings under heat stress relative to controls