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. 2021 Feb 11:12:621336.
doi: 10.3389/fmicb.2021.621336. eCollection 2021.

Transcriptomic Analysis of Wheat Seedling Responses to the Systemic Acquired Resistance Inducer N-Hydroxypipecolic Acid

Eric T Zhang  1   2 , Hao Zhang  3 , Weihua Tang  1
Affiliations

Transcriptomic Analysis of Wheat Seedling Responses to the Systemic Acquired Resistance Inducer N-Hydroxypipecolic Acid

Eric T Zhang et al. Front Microbiol. .

Abstract

The fungal pathogen Fusarium graminearum can cause destructive diseases on wheat, such as Fusarium head blight and Fusarium crown rot. However, a solution is still unavailable. Recently, N-hydroxypipecolic acid (NHP) was identified as a potent signaling molecule that is capable of inducing systemic acquired resistance to bacterial, oomycete, and fungal infection in several plant species. However, it is not clear whether NHP works in wheat to resist F. graminearum infection or how NHP affects wheat gene expression. In this report, we showed that pretreatment with NHP moderately increased wheat seedling resistance to F. graminearum. Using RNA sequencing, we found that 17% of wheat-expressed genes were significantly affected by NHP treatment. The genes encoding nucleotide-binding leucine-rich repeat immune receptors were significantly overrepresented in the group of genes upregulated by NHP treatment, while the genes encoding receptor-like kinases were not. Our results suggested that NHP treatment sensitizes a subset of the immune surveillance system in wheat seedlings, thereby facilitating wheat defense against F. graminearum infection.

Keywords: Fusarium head blight (FHB); fungal infection; immune receptor; pathogen; systemic acquired resistance; wheat.

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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
Representative images and measurements of wheat seedlings treated with water or N-hydroxypipecolic acid (NHP). (A,B) Mock-inoculated seedlings. (C,D) F. graminearum-inoculated seedlings. Black lines show examples of lesions on coleoptiles; n = 3 independent experiments. Error bars indicate the SE. An asterisk indicates a significant difference compared with the control (p < 0.05; Student’s t-test).
FIGURE 2
FIGURE 2
RNA sequencing results of wheat seedlings treated with water or N-hydroxypipecolic acid (NHP). (A) Principal component analysis (PCA) analysis of the transcriptomes of NHP-treated and water-treated wheat seedlings. (B) Volcano plot showing the distribution of differentially expressed genes. FC, fold change of NHP-treated sample with respect to mock-treated sample. False discovery rate (FDR) <0.05.
FIGURE 3
FIGURE 3
Quantitative real-time reverse transcription quantitative PCR (qRT-PCR) verification of the expression of nine wheat genes upon N-hydroxypipecolic acid (NHP) treatment. Error bars indicate the SE, n = 3.
FIGURE 4
FIGURE 4
Heatmap presentation of the top 50 upregulated genes in response to N-hydroxypipecolic acid (NHP) treatment. Normalized expression data were presented. (A) Genes in group 1 and 2. (B) Genes in group 3, 4 and 5. (C) Genes in group 6. (D) Genes in group 7 and 8.
FIGURE 5
FIGURE 5
Gene Ontology (GO) terms that were overrepresented among the upregulated genes and callose deposition in wheat coleoptiles. (A) Dot plot presentation. (B) Map presentation. (C) Representative images of aniline blue-stained wheat coleoptiles. Scale bar = 50 μm. (D) Measurements of callose signals. *Significant difference detected by Student’s t-test.
FIGURE 6
FIGURE 6
Gene Ontology (GO) terms that were overrepresented among the downregulated genes.
FIGURE 7
FIGURE 7
N-hydroxypipecolic acid (NHP) upregulated the expression of a subset of immune-related genes. Proportions of NHP-upregulated genes in families associated with immune perception, defense signaling, and immune executors. Broken line represents the percentage of NHP-upregulated genes in the whole wheat genome (120,744). The total number of genes in each category is provided on the left. The absolute numbers of NHP-upregulated genes in each category are provided on the bar. The domain structure of subclasses of upregulated nucleotide-binding domain and leucine-rich repeats (NLRs) are illustrated on the right. Asterisks indicate significant enrichment (or depletion) of gene categories in NHP-upregulated genes (**p < 0.005; *p < 0.05; chi-square test). NB-ARC, nucleotide-binding domain found in apoptotic protease activating factor 1, resistance genes, and Caenorhabditis elegans death-4 protein; LRR, leucine-rich repeats; CC, the potato virus X resistance protein N-terminal “coiled-coil” domain; WH, Winged helix DNA-binding domain; ARM, armadillo fold domain.
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