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. 2025 Feb 28:16:1537605.
doi: 10.3389/fpls.2025.1537605. eCollection 2025.

Transcriptomic analysis of two Chinese wheat landraces with contrasting Fusarium head blight resistance reveals miRNA-mediated defense mechanisms

Lijuan Wu  1   2 , Junqiang Wang  1 , Shian Shen  1 , Zaijun Yang  3 , Xinkun Hu  1
Affiliations

Transcriptomic analysis of two Chinese wheat landraces with contrasting Fusarium head blight resistance reveals miRNA-mediated defense mechanisms

Lijuan Wu et al. Front Plant Sci. .

Abstract

Introduction: Fusarium head blight (FHB), caused primarily by Fusarium graminearum (Fg), poses a significant threat to wheat production. It is necessary to deeply understand the molecular mechanisms underlying FHB resistance in wheat breeding.

Methods: In this study, the transcriptomic responses of two Chinese wheat landraces-Wuyangmai (WY, resistant) and Chinese Spring (CS, susceptible)-to F. graminearum infection were examined using RNA sequencing (RNA-seq). Differential expression of mRNAs, long non-coding RNAs (lncRNAs), circular RNAs (circRNAs), and microRNAs (miRNAs) was analyzed at 3 and 5 days post-Fg inoculation (dpi).

Results: The results showed that WY exhibited a targeted miRNA response, primarily modulating defense-related pathways such as glutathione metabolism and phenylpropanoid biosynthesis, which are crucial for oxidative stress regulation and pathogen defense response. In contrast, CS displayed a broader transcriptional response, largely linked to general metabolic processes rather than immune activation. Notably, the up-regulation of genes involved in oxidative stress and immune defense in WY confirmed its enhanced resistance to FHB. The integrated analysis of miRNA-mRNA interactions highlighted miRNAs as central regulators of defense mechanisms in WY, particularly at later stages of infection. These miRNAs targeted genes involved in immune responses, while lncRNAs and circRNAs played a more limited role in the regulation of defense responses. The GO and KEGG pathway enrichment analyses further revealed that WY enriched for plant-pathogen interaction and secondary metabolite biosynthesis pathways, which are crucial for pathogen resistance. In contrast, CS prioritized metabolic homeostasis, suggesting a less effective defense strategy.

Discussion: Overall, this study underscores the critical role of miRNA-mediated regulation in FHB resistance in WY. These insights into miRNA-mediated regulatory mechanisms provide a molecular basis for breeding FHB-resistant wheat varieties and highlight miRNA-mRNA interactions as promising targets for enhancing disease resilience.

Keywords: Fusarium head blight; RNA sequencing; Sichuan wheat landraces; circRNAs; lncRNAs; miRNAs.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Statistics of differentially expressed RNAs across various comparisons. The 0, 3, and 5-dpi represent samples collected at 0, 3, and 5 days post F. graminearum inoculation (dpi), respectively. CS and WY refer to Chinese Spring and Wuyangmai, respectively. LncRNA, long non-coding RNA; miRNA, microRNA; circRNA, circular RNA.
Figure 2
Figure 2
Expression profiles of differentially expressed RNAs at 5 dpi with F. graminearum. The outermost ring shows chromosome information, followed by mRNA (gene), lncRNA, circRNA, and miRNA. For each group of differentially expressed RNAs, red, blue, and the height indicate up-regulation, down-regulation, and significance [-log10 (FDR)], respectively.
Figure 3
Figure 3
Interaction of differentially expressed miRNAs with all miRNAs targeted by differentially expressed mRNAs, lncRNAs, and circRNAs. Here, DE_miRNA represents differentially expressed miRNAs; DE_mRNA_Target miRNA, DE_lncRNA_Target miRNA, and DE_circRNA_Target miRNA represent miRNAs targeted by differentially expressed genes, lncRNAs, and circRNAs, respectively.
Figure 4
Figure 4
Differential expression analysis for up-regulated genes. (A) Statistical analysis for all genes. (B) Volcano plot of DEGs obtained in the comparison of 3 vs. 5-dpi. (C) GO term and (D) KEGG pathway enrichment analysis for significantly up-regulated DEGs. (E) Gene expression heatmap of glutathione metabolism pathway.
Figure 5
Figure 5
Targeting relationships between DE_miRNAs and DEGs. (A) Comparison of the top 20 DE_miRNAs most relevant to target gene regulation in CS and WY. (B) Targeting relationships between the DE_miRNAs specifically expressed in CS and WY and DEGs. (C) Expression heatmap of genes significantly down-regulated by novel_miR_228 and significantly up-regulated by tae-miR1122a with molecular function (MF) GO term. Heatmap represents log2 (FC) between F. graminearum infected and control.
Figure 6
Figure 6
GO term enrichment analysis for DE_miRNA-regulated DEGs. GeneNum denotes the gene number.
Figure 7
Figure 7
KEGG pathway enrichment analysis for DE_miRNA-regulated DEGs. GeneRatio indicates the gene ratio.
Figure 8
Figure 8
Relative expression comparison for selected genes using RNA-seq and RT-qPCR data.
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