Dataset Information

Integrative analysis of the multi-omics reveals the stripe rust fungus resistance mechanism of the TaPAL in wheat.

ABSTRACT: Wheat is one of the major food crops in the world. However, stripe rust fungus significantly decreases wheat yield and quality. In the present study, transcriptomic and metabolite analyses were conducted in R88 (resistant line) and CY12 (susceptible cultivar) during Pst-CYR34 infection due to the limited availability of information regarding the underlying mechanisms governing wheat-pathogen interactions. The results revealed that Pst infection promoted the genes and metabolites involved in phenylpropanoid biosynthesis. The key enzyme gene TaPAL to regulate lignin and phenolic synthesis has a positive resistance contribution to Pst in wheat, which was verified by the virus-induced gene silencing (VIGS) technique. The distinctive resistance of R88 is regulated by the selective expression of genes involved in the fine-tuning of wheat-Pst interactions. Furthermore, metabolome analysis suggested that lignin biosynthesis-related metabolite accumulation was significantly affected by Pst. These results help to elucidate the regulatory networks of wheat-Pst interactions and pave the way for durable resistance breeding in wheat, which may ease environmental and food crises around the world.

SUBMITTER: Liu R

PROVIDER: S-EPMC10277697 | biostudies-literature | 2023

REPOSITORIES: biostudies-literature

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Integrative analysis of the multi-omics reveals the stripe rust fungus resistance mechanism of the <i>TaPAL</i> in wheat.

Liu Rong R Lv Xue X Wang Xiaohua X Yang Li L Cao Jun J Dai Ya Y Wu Wang W Wu Yu Y

Frontiers in plant science 20230605

Wheat is one of the major food crops in the world. However, stripe rust fungus significantly decreases wheat yield and quality. In the present study, transcriptomic and metabolite analyses were conducted in R88 (resistant line) and CY12 (susceptible cultivar) during Pst-CYR34 infection due to the limited availability of information regarding the underlying mechanisms governing wheat-pathogen interactions. The results revealed that Pst infection promoted the genes and metabolites involved in phen ...[more]

PMID: 37342140

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Project description:Protein phosphorylation plays an important role in immune signaling transduction in plant resistance to pathogens. Wheat stripe rust, caused by Puccinia striiformis f. sp. tritici (Pst), severely devastates wheat production. Nonetheless, the molecular mechanism of wheat resistance to stripe rust remains limited. In this study, quantitative phosphoproteomics was employed to investigate the protein phosphorylation changes in wheat challenged by Pst. A total of 1537 and 2470 differentially accumulated phosphoproteins (DAPs) were identified from four early infection stage (6, 12, 18 and 24 h post-inoculation) in incompatible and compatible wheat-Pst interactions respectively. KEGG analysis revealed that Oxidative Phosphorylation, Phosphatidylinositol Signaling, and MAPK signaling processes are distinctively enriched in incompatible interaction, while Biosynthesis of secondary metabolites and RNA degradation process were significantly enriched in compatible interactions. In particular, abundant changes in phosphorylation levels of chloroplast proteins were identified, suggesting the regulatory role of photosynthesis in wheat-Pst interaction, which is further emphasized by protein-protein interaction (PPI) network analysis. Motif-x analysis identified [xxxxSPxxxx] motif, likely phosphorylation sites for defensive response-related kinases, and a new [xxxxSSxxxx] motif significantly enriched in incompatible interaction. The results shed light on the early phosphorylation events contributing to wheat resistance against Pst. Moreover, our study demonstrated that the phosphorylation levels of Nucleoside diphosphate kinase TaNAPK1 are upregulated at 12 hpi with CYR23 and at 24 hpi with CYR31. Transient silencing of TaNAPK1 was able to attenuate wheat resistance to CYR23 and CYR31. Our study provides new insights into the mechanisms underlying Pst-wheat interactions and may provide database to find potential targets for the development of new resistant varieties.

Project description:IntroductionContinuous identification and application of novel resistance genes against stripe rust are of great importance for wheat breeding. Wild emmer wheat, Triticum dicoccoides, has adapted to a broad range of environments and is a valuable genetic resource that harbors important beneficial traits, including resistance to stripe rust caused by Puccinia striiformis f. sp. tritici (Pst). However, there has been a lack of systematic exploration of genes against Pst races in wild emmer wheat.MethodsGenome-wide transcriptome profiles were conducted on two wild emmer wheat genotypes with different levels of resistance to (Pst (DR3 exhibiting moderate (Pst resistance, and D7 displaying high (Pst resistance). qRT-PCR was performed to verify findings by RNA-seq.ResultsA higher number of DEGs were identified in the moderately (Pst-resistant genotype, while the highly (Pst-resistant genotype exhibited a greater enrichment of pathways. Nonetheless, there were consistent patterns in the enrichment of pathways between the two genotypes at the same time of inoculation. At 24 hpi, a majority of pathways such as the biosynthesis of secondary metabolites, phenylpropanoid biosynthesis, phenylalanine metabolism, and alpha-Linolenic acid metabolism exhibited significant enrichment in both genotypes. At 72 hpi, the biosynthesis of secondary metabolites and circadian rhythm-plant pathways were notably and consistently enriched in both genotypes. The majority of (WRKY, MADs , and AP2-ERF families were found to be involved in the initial stage of response to Pst invasion (24 hpi), while the MYB, NAC, TCP, and b-ZIP families played a role in defense during the later stage of Pst infection (72 hpi).DiscussionIn this present study, we identified numerous crucial genes, transcription factors, and pathways associated with the response and regulation of wild emmer wheat to Pst infection. Our findings offer valuable information for understanding the function of crucial Pst-responsive genes, and will deepen the understanding of the complex resistance mechanisms against Pst in wheat.

Project description:BackgroundWheat stripe rust, caused by Puccinia striiformis f. sp. tritici, is a costly global disease that burdens farmers with yield loss and high fungicide expenses. This sophisticated biotrophic parasite infiltrates wheat leaves and develops infection structures inside host cells, appropriating nutrients while suppressing the plant defense response. Development in most eukaryotes is regulated by small RNA molecules, and the success of host-induced gene silencing technology in Puccinia spp. implies the existence of a functional RNAi system. However, some fungi lack this capability, and small RNAs have not yet been reported in rust fungi. The objective of this study was to determine whether P. striiformis carries an endogenous small RNA repertoire.ResultsWe extracted small RNA from rust-infected wheat flag leaves and performed high-throughput sequencing. Two wheat cultivars were analyzed: one is susceptible; the other displays partial high-temperature adult plant resistance. Fungal-specific reads were identified by mapping to the P. striiformis draft genome and removing reads present in uninfected control libraries. Sequencing and bioinformatics results were verified by RT-PCR. Like other RNAi-equipped fungi, P. striiformis produces large numbers of 20-22 nt sequences with a preference for uracil at the 5' position. Precise post-transcriptional processing and high accumulation of specific sRNA sequences were observed. Some predicted sRNA precursors possess a microRNA-like stem-loop secondary structure; others originate from much longer inverted repeats containing gene sequences. Finally, sRNA-target prediction algorithms were used to obtain a list of putative gene targets in both organisms. Predicted fungal target genes were enriched for kinases and small secreted proteins, while the list of wheat targets included homologs of known plant resistance genes.ConclusionsThis work provides an inventory of small RNAs endogenous to an important plant pathogen, enabling further exploration of gene regulation on both sides of the host/parasite interaction. We conclude that small RNAs are likely to play a role in regulating the complex developmental processes involved in stripe rust pathogenicity.

Dataset Information

Integrative analysis of the multi-omics reveals the stripe rust fungus resistance mechanism of the TaPAL in wheat.

Publications

Integrative analysis of the multi-omics reveals the stripe rust fungus resistance mechanism of the <i>TaPAL</i> in wheat.

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