Stripe rust is a devastating fungal disease that afflicts wheat in many regions of the world. New races of Puccinia striiformis, the pathogen responsible for this disease, have overcome most of the known race-specific resistance genes. We report the map-based cloning of the gene Yr36 (WKS1), which confers resistance to a broad spectrum of stripe rust races at relatively high temperatures (25 degrees to 35 degrees C). This gene includes a kinase and a putative START lipid-binding domain. Five independent mutations and transgenic complementation confirmed that both domains are necessary to confer resistance. Yr36 is present in wild wheat but is absent in modern pasta and bread wheat varieties, and therefore it can now be used to improve resistance to stripe rust in a broad set of varieties.
New races of Puccinia striiformis f. sp. tritici (Pst), the causal pathogen of wheat stripe rust, show high virulence to previously deployed resistance genes and are responsible for large yield losses worldwide. To identify new sources of resistance we performed a genome-wide association study (GWAS) using a worldwide collection of 1000 spring wheat accessions. Adult plants were evaluated under field conditions in six environments in the western United States, and seedlings were tested with four Pst races. A single-nucleotide polymorphism (SNP) Infinium 9K-assay provided 4585 SNPs suitable for GWAS. High correlations among environments and high heritabilities were observed for stripe rust infection type and severity. Greater levels of Pst resistance were observed in a subpopulation from Southern Asia than in other groups. GWAS identified 97 loci that were significant for at least three environments, including 10 with an experiment-wise adjusted Bonferroni probability < 0.10. These 10 quantitative trait loci (QTL) explained 15% of the phenotypic variation in infection type, a percentage that increased to 45% when all QTL were considered. Three of these 10 QTL were mapped far from previously identified Pst resistance genes and QTL, and likely represent new resistance loci. The other seven QTL mapped close to known resistance genes and allelism tests will be required to test their relationships. In summary, this study provides an integrated view of stripe rust resistance resources in spring wheat and identifies new resistance loci that will be useful to diversify the current set of resistance genes deployed to control this devastating disease.
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BackgroundWheat yellow (stripe) rust caused by Puccinia striiformis f. sp. tritici (PST) is one of the most devastating diseases of wheat worldwide. To design effective breeding strategies that maximize the potential for durable disease resistance it is important to understand the molecular basis of PST pathogenicity. In particular, the characterisation of the structure, function and evolutionary dynamics of secreted effector proteins that are detected by host immune receptors can help guide and prioritize breeding efforts. However, to date, our knowledge of the effector repertoire of cereal rust pathogens is limited.ResultsWe re-sequenced genomes of four PST isolates from the US and UK to identify effector candidates and relate them to their distinct virulence profiles. First, we assessed SNP frequencies between all isolates, with heterokaryotic SNPs being over tenfold more frequent (5.29 ± 2.23 SNPs/kb) than homokaryotic SNPs (0.41 ± 0.28 SNPs/kb). Next, we implemented a bioinformatics pipeline to integrate genomics, transcriptomics, and effector-focused annotations to identify and classify effector candidates in PST. RNAseq analysis highlighted transcripts encoding secreted proteins that were significantly enriched in haustoria compared to infected tissue. The expression of 22 candidate effector genes was characterised using qRT-PCR, revealing distinct temporal expression patterns during infection in wheat. Lastly, we identified proteins that displayed non-synonymous substitutions specifically between the two UK isolates PST-87/7 and PST-08/21, which differ in virulence to two wheat varieties. By focusing on polymorphic variants enriched in haustoria, we identified five polymorphic effector candidates between PST-87/7 and PST-08/21 among 2,999 secreted proteins. These allelic variants are now a priority for functional validation as virulence/avirulence effectors in the corresponding wheat varieties.ConclusionsIntegration of genomics, transcriptomics, and effector-directed annotation of PST isolates has enabled us to move beyond the single isolate-directed catalogues of effector proteins and develop a framework for mining effector proteins in closely related isolates and relate these back to their defined virulence profiles. This should ultimately lead to more comprehensive understanding of the PST pathogenesis system, an important first step towards developing more effective surveillance and management strategies for one of the most devastating pathogens of wheat.
Stripe rust appears as a mass of yellow to orange urediniospores erupting from pustules arranged in long, narrow stripes on leaves (usually between veins), leaf sheaths, glumes and awns on susceptible plants. Resistant wheat cultivars are characterized by various infection types from no visual symptoms to small hypersensitive flecks to uredinia surrounded by chlorosis or necrosis with restricted urediniospore production. On seedlings, uredinia produced by the infection of a single urediniospore are not confined by leaf veins, but progressively emerge from the infection site in all directions, potentially covering the entire leaf surface. Individual uredinial pustules are oblong, 0.4-0.7 mm in length and 0.1 mm in width. Urediniospores are broadly ellipsoidal to broadly obovoid, (16-)18-30(-32) × (15-)17-27(-28) μm, with a mean of 24.5 × 21.6 μm, yellow to orange in colour, echinulate, and with 6-18 scattered germ pores. Urediniospores can germinate rapidly when free moisture (rain or dew) occurs on leaf surfaces and when the temperatures range is between 7 and 12 °C. At higher temperatures or during the later growing stages of the host, black telia are often produced, which are pulvinate to oblong, 0.2-0.7 mm in length and 0.1 mm in width. The teliospores are predominantly two-celled, dark brown with thick walls, mostly oblong-clavate, (24-)31-56(-65) × (11-)14-25(-29) μm in length and width, and rounded or flattened at the apex.
Stripe rust, caused by Puccinia striiformis f. sp. tritici (Pst), is one of the most destructive diseases of wheat. Here we report a 110-Mb draft sequence of Pst isolate CY32, obtained using a ‘fosmid-to-fosmid’ strategy, to better understand its race evolution and pathogenesis. The Pst genome is highly heterozygous and contains 25,288 protein-coding genes. Compared with non-obligate fungal pathogens, Pst has a more diverse gene composition and more genes encoding secreted proteins. Re-sequencing analysis indicates significant genetic variation among six isolates collected from different continents. Approximately 35% of SNPs are in the coding sequence regions, and half of them are non-synonymous. High genetic diversity in Pst suggests that sexual reproduction has an important role in the origin of different regional races. Our results show the effectiveness of the ‘fosmid-to-fosmid’ strategy for sequencing dikaryotic genomes and the feasibility of genome analysis to understand race evolution in Pst and other obligate pathogens.
High-temperature adult-plant (HTAP) resistance expresses when plants grow old and the weather becomes warm. This non-race specific and durable type of resistance has been used successfully in control of wheat stripe rust in the US since early 1960s. This article describes practical procedures for identification and characterization of HTAP resistance and reviews recent studies on discovery of genes conferring HTAP resistance. Recent studies providing insights to the molecular basis for the durability of HTAP resistance will be presented. Strategies for improving levels of HTAP resistance and improving control of stripe rust through combining HTAP resistance with effective all-stage resistance will be discussed.
In China, wheat stripe rust, caused by Puccinia striiformis f. sp. tritici, is one of the most destructive diseases of wheat and can cause severe yield losses when susceptible cultivars are grown and weather conditions are favorable for the disease. Wheat stripe rust most frequently affects the winter wheat growing areas in Northwest, Southwest, and North China, and the spring wheat growing areas in Northwest China. In the 2001-2002 growing season, a widespread stripe rust epidemic affected about 6.6 million hectares of wheat in 11 provinces: Si-chuan, Chongqing, eastern Gansu, southern and western Shaanxi, southern and central Ningxia, Yunnan, Guizhou, Hubei, Henan, southern and central Hebei, and Shandong. The epidemic could be attributed to relatively warm weather from November 2001 to March 2002, high frequencies of stripe rust races CYR31 and CYR32, and widely grown susceptible cultivars. Race CYR31 was virulent on the Chinese differential cultivars Trigo Eureka, Fulhard, Lutescens 128, Mentana, Virgilio, Abbondanza, Early Premium, Funo, Danish 1, Fengchan 3, Lovrin 13, Shui-yuan 11, Lovrin 10, and Hybrid 46. Race CYR32 had all the virulence factors of CYR31, plus virulences on Chinese differential cultivars Jubilejina 2 and Kangyin 655, i.e., CYR32 was virulent on all differential cultivars, except Zhong 4. When tested on the world and European differential and some other resistant genotypes, CYR32 was virulent on Chinese 166 (Yr1), Heines VII (Yr2, Yr25, and YrHVII), Vilmorin 23 (Yr3a and Yr4a), Heines Kolben (Yr6 and YrHK), Lee (Yr7, Yr22, and Yr23), Clement (Yr9, Yr25, YrCle), VPM1 (Yr17), Selkirk (Yr27), Anza (YrA), Carstens V (YrCV1, YrCV2, and YrCV3), Gaby (YrG), Strubes Dickkopf (Yr25), and Suwon 92/Omar (YrSO). Resistance genes in Triticum spelta album (Yr5), Zhong 4, and Moro (Yr10 and YrMor) were effective against all races identified.
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