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Single amino acid change alters specificity of the multi-allelic wheat stem rust resistance locus SR9.

ABSTRACT: Most rust resistance genes thus far isolated from wheat have a very limited number of functional alleles. Here, we report the isolation of most of the alleles at wheat stem rust resistance gene locus SR9. The seven previously reported resistance alleles (Sr9a, Sr9b, Sr9d, Sr9e, Sr9f, Sr9g, and Sr9h) are characterised using a synergistic strategy. Loss-of-function mutants and/or transgenic complementation are used to confirm Sr9b, two haplotypes of Sr9e (Sr9e_h1 and Sr9e_h2), Sr9g, and Sr9h. Each allele encodes a highly related nucleotide-binding site leucine-rich repeat (NB-LRR) type immune receptor, containing an unusual long LRR domain, that confers resistance to a unique spectrum of isolates of the wheat stem rust pathogen. The only SR9 protein effective against stem rust pathogen race TTKSK (Ug99), SR9H, differs from SR9B by a single amino acid. SR9B and SR9G resistance proteins are also distinguished by only a single amino acid. The SR9 allelic series found in the B subgenome are orthologs of wheat stem rust resistance gene Sr21 located in the A subgenome with around 85% identity in protein sequences. Together, our results show that functional diversification of allelic variants at the SR9 locus involves single and multiple amino acid changes that recognize isolates of wheat stem rust.

SUBMITTER: Zhang J

PROVIDER: S-EPMC10645757 | biostudies-literature | 2023 Nov

REPOSITORIES: biostudies-literature

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Single amino acid change alters specificity of the multi-allelic wheat stem rust resistance locus SR9.

Zhang Jianping J Nirmala Jayaveeramuthu J Chen Shisheng S Jost Matthias M Steuernagel Burkhard B Karafiatova Mirka M Hewitt Tim T Li Hongna H Edae Erena E Sharma Keshav K Hoxha Sami S Bhatt Dhara D Antoniou-Kourounioti Rea R Dodds Peter P Wulff Brande B H BBH Dolezel Jaroslav J Ayliffe Michael M Hiebert Colin C McIntosh Robert R Dubcovsky Jorge J Zhang Peng P Rouse Matthew N MN Lagudah Evans E

Nature communications 20231114 1

Most rust resistance genes thus far isolated from wheat have a very limited number of functional alleles. Here, we report the isolation of most of the alleles at wheat stem rust resistance gene locus SR9. The seven previously reported resistance alleles (Sr9a, Sr9b, Sr9d, Sr9e, Sr9f, Sr9g, and Sr9h) are characterised using a synergistic strategy. Loss-of-function mutants and/or transgenic complementation are used to confirm Sr9b, two haplotypes of Sr9e (Sr9e_h1 and Sr9e_h2), Sr9g, and Sr9h. Each ...[more]

PMID: 37963867

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Project description:Aim:To characterise a recently discovered stem rust resistance locus on wheat chromosome 7AL. Transcriptome analysis by RNA-sequencing, in association with microscopic observations, was used to compare responses to the Puccinia graminis f. sp. tritici pathogen of the susceptible line Columbus, and two independent backcrossed resistant lines containing the locus, Columbus-NS765 and Columbus-NS766. Results: Microscopic observations of infected leaves revealed that the resistance conferred by the 7AL resistance locus was initiated by two days post-inoculation, upon the entry of the stem rust fungus into the plant through the stoma. Death of guard and epidermal cells adjacent to the fungal points of entry was observed to be clearly more frequent in resistant lines than in the susceptible genotype, suggesting that the resistance response is similar in all genotypes, but enhanced in the resistant lines. Transcriptomic analysis, combined with assignment of genes to wheat chromosomes, revealed a disporportionately high number of differentially expressed genes were located on chromosomes 7AL and 6A. A number of genes annotated as cysteine-rich receptor-like kinases were located on chromosome 7AL. Closer investigation indicated that the encoded proteins were in fact putative receptor-like cytoplasmic kinases (RLCKs). One of the putative RLCK genes contained a SNP marker previously shown to co-segregate with the 7AL resistance locus. The large number of differentially expressed genes on chromosome 6A indicated the presence of a large introgression on this chromosome that co-segregated with stem rust resistance in the two independent resistant lines, but its role in the resistance response is currently unclear. Conclusions: This study represents the first transcriptome analysis of responses to stem rust in wheat, and the first investigation of the resistance conferred by the newly-discovered wheat 7AL stem rust resistance locus. Microscopy showed the resistance response was associated with pre-haustorial cell death. Results of the RNA-seq, which has the resolution to discriminate between homeologous wheat genes, along with assignment of differentially expressed genes to wheat chromosomes, suggested putative receptor-like cytoplasmic kinases linked to the 7AL locus as candidate resistance genes for further investigation.

Project description:BackgroundThe adult plant stem rust resistance gene Sr2 was introgressed into hexaploid wheat cultivar (cv) Marquis from tetraploid emmer wheat cv Yaroslav, to generate stem rust resistant cv Hope in the 1920s. Subsequently, Sr2 has been widely deployed and has provided durable partial resistance to all known races of Puccinia graminis f. sp. tritici. This report describes the physical map of the Sr2-carrying region on the short arm of chromosome 3B of cv Hope and compares the Hope haplotype with non-Sr2 wheat cv Chinese Spring.ResultsSr2 was located to a region of 867 kb on chromosome 3B in Hope, which corresponded to a region of 567 kb in Chinese Spring. The Hope Sr2 region carried 34 putative genes but only 17 were annotated in the comparable region of Chinese Spring. The two haplotypes differed by extensive DNA sequence polymorphisms between flanking markers as well as by a major insertion/deletion event including ten Germin-Like Protein (GLP) genes in Hope that were absent in Chinese Spring. Haplotype analysis of a limited number of wheat genotypes of interest showed that all wheat genotypes carrying Sr2 possessed the GLP cluster; while, of those lacking Sr2, some, including Marquis, possessed the cluster, while some lacked it. Thus, this region represents a common presence-absence polymorphism in wheat, with presence of the cluster not correlated with presence of Sr2. Comparison of Hope and Marquis GLP genes on 3BS found no polymorphisms in the coding regions of the ten genes but several SNPs in the shared promoter of one divergently transcribed GLP gene pair and a single SNP downstream of the transcribed region of a second GLP.ConclusionPhysical mapping and sequence comparison showed major haplotype divergence at the Sr2 locus between Hope and Chinese Spring. Candidate genes within the Sr2 region of Hope are being evaluated for the ability to confer stem rust resistance. Based on the detailed mapping and sequencing of the locus, we predict that Sr2 does not belong to the NB-LRR gene family and is not related to previously cloned, race non-specific rust resistance genes Lr34 and Yr36.

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Single amino acid change alters specificity of the multi-allelic wheat stem rust resistance locus SR9.

Publications

Single amino acid change alters specificity of the multi-allelic wheat stem rust resistance locus SR9.

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