Abstract
The leaf rust pathogen, Puccinia triticina (Pt), threatens global wheat production. The deployment of leaf rust (Lr) resistance (R) genes in wheat varieties is often followed by the development of matching virulence in Pt due to presumed changes in avirulence (Avr) genes in Pt. Identifying such Avr genes is a crucial step to understand the mechanisms of wheat-rust interactions. This study is the first to develop and apply an integrated framework of gene expression, single nucleotide polymorphism (SNP), insertion/deletion (InDel), and copy number variation (CNV) analysis in a rust fungus and identify candidate avirulence genes. Using a long-read based de novo genome assembly of an isolate of Pt (‘Pt104’) as the reference, whole-genome resequencing data of 12 Pt pathotypes derived from three lineages Pt104, Pt53, and Pt76 were analyzed. Candidate avirulence genes were identified by correlating virulence profiles with small variants (SNP and InDel) and CNV, and RNA-seq data of an additional three Pt isolates to validate expression of genes encoding secreted proteins (SPs). Out of the annotated 29,043 genes, 2392 genes were selected as SP genes with detectable expression levels. Small variant comparisons between the isolates identified 27–40 candidates and CNV analysis identified 14–31 candidates for each Avr gene, which when combined, yielded the final 40, 64, and 69 candidates for AvrLr1, AvrLr15, and AvrLr24, respectively. Taken together, our results will facilitate future work on experimental validation and cloning of Avr genes. In addition, the integrated framework of data analysis that we have developed and reported provides a more comprehensive approach for Avr gene mining than is currently available.
Highlights
Leaf rust, caused by Puccinia triticina (Pt), is the most widespread rust disease of wheat and the most damaging biotic stress of wheat globally, causing losses of around 3.25% globally [1]
To further validate the predicted secreted proteins (SPs), RNA sequence data for two isolates that were avirulent on Lr1, Lr15, and Lr24 (S96 and S108) and one isolate that was avirulent on Lr15 and Lr24 (S473) were used to select the SPs with detectable expression
The leaf rust fungus Pt is the most widely distributed wheat rust pathogen worldwide and is responsible for most of the wheat crop yield loss arising from rust [1]
Summary
Leaf rust, caused by Puccinia triticina (Pt), is the most widespread rust disease of wheat and the most damaging biotic stress of wheat globally, causing losses of around 3.25% globally [1]. The deployment of leaf rust (Lr) resistance (R) genes in wheat varieties is the most effective and economical method for reducing yield losses and ensuring adequate quantities of pesticide-free food. In addressing this challenge, it is crucial to get a better understanding of the genetic basis of wheat-rust interactions at the molecular level. Pathogen-associated molecular patterns (PAMPs) are recognized by plant pattern recognition receptors (PRRs), resulting in PAMP-triggered immunity (PTI). A pathogen may breach PTI by deploying effectors (secreted proteins) that modify plant metabolism and defense response, and in turn, the plant host may evolve resistance proteins that recognize pathogen effectors either directly [8] or indirectly [9] and result in effector-triggered immunity (ETI). The host ETI response can be evaded by a pathogen through modification of avirulence (Avr) genes, with the selection force driving the coevolution of R genes in plants and Avr genes in pathogens
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