Comparative Transcriptome Analysis Reveals the Gene Expression and Regulatory Characteristics of Broad-Spectrum Immunity to Leaf Rust in a Wheat–Agropyron cristatum 2P Addition Line

Abstract

Wheat leaf rust (caused by Puccinia triticina Erikss.) is among the major diseases of common wheat. The lack of resistance genes to leaf rust has limited the development of wheat cultivars. Wheat–Agropyron cristatum (A. cristatum) 2P addition line II-9-3 has been shown to provide broad-spectrum immunity to leaf rust. To identify the specific A. cristatum resistance genes and related regulatory pathways in II-9-3, we conducted a comparative transcriptome analysis of inoculated and uninoculated leaves of the resistant addition line II-9-3 and the susceptible cultivar Fukuhokomugi (Fukuho). The results showed that there were 66 A. cristatum differentially expressed genes (DEGs) and 1389 wheat DEGs in II-9-3 during P. triticina infection. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment and gene set enrichment analysis (GSEA) revealed that the DEGs of II-9-3 were associated with plant–pathogen interaction, MAPK signaling pathway–plant, plant hormone signal transduction, glutathione metabolism, and phenylpropanoid biosynthesis. Furthermore, many defense-related A. cristatum genes, such as two NLR genes, seven receptor kinase-encoding genes, and four transcription factor-encoding genes, were identified. Our results indicated that the key step of resistance to leaf rust involves, firstly, the gene expression of chromosome 2P upstream of the immune pathway and, secondly, the effect of chromosome 2P on the co-expression of wheat genes in II-9-3. The disease resistance regulatory pathways and related genes in the addition line II-9-3 thus could play a critical role in the effective utilization of innovative resources for leaf rust resistance in wheat breeding.

Leaf rust (Puccinia recondita f. sp. secalis) triggers substantial changes in rye (Secale cereale L.) at the transcriptome and metabolome levels

“…In recent years, RNA-seq analyses have become common in various biological research fields. For example, it has been used to identify plant resistance genes [ 14 , 15 ]. To identify the significant DEGs, we analyzed the transcriptomic data using the following strict selection criteria to eliminate the genes with only a minor role in the rye defense response to LR: FDR < 0.01, |log 2 (fold-change)| ≥ 2, and BM > 50.…”

“…Although transcriptome analyses are typically conducted using less restrictive criteria (e.g., FDR < 0.05 and |log 2 (fold-change)| ≥ 0.5–1) [e.g. [ 14 , 15 , 55 ]], some previous studies used similarly strict selection criteria. For example, Coram et al [ 56 ] used strict selection criteria to analyze the transcripts associated with race-specific resistance to stripe rust in wheat.…”

“…Transcriptome sequencing (RNA-seq) is a powerful experimental technique for exploring global changes in gene expression in response to various stimuli (e.g., developmental changes and responses to abiotic and biotic stresses) [ 12 ]. It has been widely used for studying plant host–pathogen interactions and various diseases, including LR [ 13 – 15 ] in wheat, which is a close relative of rye. Poretti et al [ 14 ] identified 753 genes with expression levels that were uniquely down-regulated in the susceptible isogenic line Thatcher following an infection with LR and powdery mildew.…”

“…Ji et al [ 15 ] identified 1,455 differentially expressed genes (DEGs) in the wheat– Agropyron cristatum 2P addition line II-9-3 infected with LR; most of these DEGs were wheat genes. The Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis and gene set enrichment analysis (GSEA) assigned the DEGs to several pathways, including the following: plant–pathogen interaction, MAPK signaling pathway–plant, plant hormone signal transduction, glutathione metabolism, and phenylpropanoid biosynthesis.…”

The Genomic Variation and Differentially Expressed Genes on the 6P Chromosomes in Wheat–Agropyron cristatum Addition Lines 5113 and II-30-5 Confer Different Desirable Traits

“…Introgression of the A. cristatum 1P chromosome reduces leaf size and plant height to improve the plant architecture of common wheat [ 19 ]. The A. cristatum 2P and 3P chromosomes carry genes for broad-spectrum immunity to leaf rust and high resistance to powdery mildew [ 20 , 21 ]. The A. cristatum 5P chromosome affects homologous chromosome pairing [ 22 ], and the A. cristatum 6P chromosome confers many high-yield related traits to common wheat, such as multiple florets, higher grain number per spike (GNS), and multiple fertile tiller numbers [ 23 , 24 , 25 ].…”