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Crop losses caused by plant pathogens are a primary threat to stable food production. Stripe rust (Puccinia striiformis) is a fungal pathogen of cereal crops that causes significant, persistent yield loss. Stripe rust exhibits host species specificity, with lineages that have adapted to infect wheat and barley. While wheat stripe rust and barley stripe rust are commonly restricted to their corresponding hosts, the genes underlying this host specificity remain unknown. Here, we show that three resistance genes, Rps6, Rps7, and Rps8, contribute to immunity in barley to wheat stripe rust. Rps7 cosegregates with barley powdery mildew resistance at the Mla locus. Using transgenic complementation of different Mla alleles, we confirm allele-specific recognition of wheat stripe rust by Mla. Our results show that major resistance genes contribute to the host species specificity of wheat stripe rust on barley and that a shared genetic architecture underlies resistance to the adapted pathogen barley powdery mildew and non-adapted pathogen wheat stripe rust., The genes underlying stripe rust host specificity between wheat and barley remain unknown. Here, the authors report that Rps6, Rps7 and Rps8 determine host species specificity in barley at different stages of the pathogen lifecycle and the barley powdery mildew immune receptor Mla8 and Rps7 are the same gene.

Transcriptomics is being increasingly applied to generate new insight into the interactions between plants and their pathogens. For the wheat yellow (stripe) rust pathogen (Puccinia striiformis f. sp. tritici, Pst) RNA-based sequencing (RNA-Seq) has proved particularly valuable, overcoming the barriers associated with its obligate biotrophic nature. This includes the application of RNA-Seq approaches to study Pst and wheat gene expression dynamics over time and the Pst population composition through the use of a novel RNA-Seq based surveillance approach called “field pathogenomics”. As a dual RNA-Seq approach, the field pathogenomics technique also provides gene expression data from the host, giving new insight into host responses. However, this has created a wealth of data for interrogation. Results: Here, we used the field pathogenomics approach to generate 538 new RNA-Seq datasets from Pst-infected field wheat samples, doubling the amount of transcriptomics data available for this important pathosystem. We then analysed these datasets alongside 66 RNA-Seq datasets from four Pst infection time-courses and 420 Pst-infected plant field and laboratory samples that were publicly available. A database of gene expression values for Pst and wheat was generated for each of these 1024 RNA-Seq datasets and incorporated into the development of the rust expression browser (http://www.rust-expression.com). This enables for the first time simultaneous ‘point-and-click’ access to gene expression profiles for Pst and its wheat host and represents the largest database of processed RNA-Seq datasets available for any of the three Puccinia wheat rust pathogens. We also demonstrated the utility of the browser through investigation of expression of putative Pst virulence genes over time and examined the host plants response to Pst infection. Conclusions: The rust expression browser offers immense value to the wider community, facilitating data sharing and transparency and the underlying database can be continually expanded as more datasets become publicly available. EEA Bordenave Fil: Adams, Thomas M.. John Innes Centre. Norwich Research Park; Reino Unido Fil: Olsson, Tjelvar S.G. John Innes Centre. Norwich Research Park; Reino Unido Fil: Ramírez-González, Ricardo H. John Innes Centre. Norwich Research Park; Reino Unido Fil: Bryant, Ruth. RAGT Seeds Ltd.; Reino Unido Fil: Bryson, Rosie. BASF SE. Agricultural Centre; Alemania Fil: Campos, Pablo Eduardo. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Agropecuaria Bordenave; Argentina Fil: Fenwick, Paul. Limagrain UK Ltd.; Reino Unido Fil: Feuerhelm, David. Syngenta Seeds Ltd.; Reino Unido Fil: Hayes, Charlotte. Elsoms Wheat Ltd.; Reino Unido Fil: Henriksson, Tina. Lantmännen Lantbruk; Suecia Fil: Hubbard, Amelia. NIAB; Reino Unido Fil: Jevtić, Radivoje. Institute of Field and Vegetable Crops; Serbia Fil: Judge, Christopher. NIAB; Reino Unido Fil: Kerton, Matthew. DSV United Kingdom Ltd.; Reino Unido Fil: Lage, Jacob. KWS UK Limited; Reino Unido Fil: Lewis, Clare M. John Innes Centre. Norwich Research Park; Reino Unido Fil: Lilly, Christine. Frontier Agriculture; Reino Unido Fil: Meidan, Udi. Hazera Seeds Ltd.; Israel Fil: Novoselović, Dario. Agricultural Institute Osijek; Croacia Fil: Patrick, Colin. Masstock Arable (UK) Ltd.; Reino Unido Fil: Wanyera, Ruth. Kenya Agricultural and Livestock Research Organization; Kenia Fil: Saunders, Diane G.O. John Innes Centre. Norwich Research Park; Reino Unido

Multilayered defense responses ensure that plants are hosts to only a few adapted pathogens in the environment. The host range of a plant pathogen depends on its ability to fully overcome plant defense barriers, with failure at any single step sufficient to prevent life cycle completion of the pathogen. Puccinia striiformis, the causal agent of stripe rust (=yellow rust), is an agronomically important obligate biotrophic fungal pathogen of wheat and barley. It is generally unable to complete its life cycle on the non-adapted wild grass species Brachypodium distachyon, but natural variation exists for the degree of hyphal colonization by Puccinia striiformis. Using three B. distachyon mapping populations, we identified genetic loci conferring colonization resistance to wheat-adapted and barley-adapted isolates of P. striiformis. We observed a genetic architecture composed of two major effect QTLs (Yrr1 and Yrr3) restricting the colonization of P. striiformis. Isolate specificity was observed for Yrr1, whereas Yrr3 was effective against all tested P. striiformis isolates. Plant immune receptors of the nucleotide binding, leucine-rich repeat (NB-LRR) encoding gene family are present at the Yrr3 locus, whereas genes of this family were not identified at the Yrr1 locus. While it has been proposed that resistance to adapted and non-adapted pathogens are inherently different, the observation of (1) a simple genetic architecture of colonization resistance, (2) isolate specificity of major and minor effect QTLs, and (3) NB-LRR encoding genes at the Yrr3 locus suggest that factors associated with resistance to adapted pathogens are also critical for non-adapted pathogens., Author summary Plants are constantly exposed to a multitude of potential pathogens but remain immune to most of these due to a multilayered immune system. Pathogens have specialized by adapting to certain host plants and their defense barriers. Most of our understanding of plant-pathogen interactions stems from these highly specialized interactions, because they are characterized by qualitative interactions (resistant or susceptible). It has generally been assumed that the genetic and molecular basis of resistance to non-adapted pathogens is fundamentally different, as either no variation exists in a species (complete immunity) or variation encompasses only early pathogen invasion (colonization), but not full susceptibility. We have studied the interaction between the agronomically important fungal stripe rust pathogen (Puccinia striiformis) of wheat and barley with the wild grass species Brachypodium distachyon. Rust infections consist of two stages: colonization of plant tissues followed by a reproductive phase. We identified natural variation for the degree of P. striiformis colonization in different B. distachyon accessions and dissected the genetic architecture controlling resistance at this infection stage. QTLs conferring resistance possessed several characteristics similar to adapted host systems, indicating that resistance to adapted and non-adapted pathogens are not intrinsically different.

Background Emerging and re-emerging pathogens imperil public health and global food security. Responding to these threats requires improved surveillance and diagnostic systems. Despite their potential, genomic tools have not been readily applied to emerging or re-emerging plant pathogens such as the wheat yellow (stripe) rust pathogen Puccinia striiformis f. sp. tritici (PST). This is due largely to the obligate parasitic nature of PST, as culturing PST isolates for DNA extraction remains slow and tedious. Results To counteract the limitations associated with culturing PST, we developed and applied a field pathogenomics approach by transcriptome sequencing infected wheat leaves collected from the field in 2013. This enabled us to rapidly gain insights into this emerging pathogen population. We found that the PST population across the United Kingdom (UK) underwent a major shift in recent years. Population genetic structure analyses revealed four distinct lineages that correlated to the phenotypic groups determined through traditional pathology-based virulence assays. Furthermore, the genetic diversity between members of a single population cluster for all 2013 PST field samples was much higher than that displayed by historical UK isolates, revealing a more diverse population of PST. Conclusions Our field pathogenomics approach uncovered a dramatic shift in the PST population in the UK, likely due to a recent introduction of a diverse set of exotic PST lineages. The methodology described herein accelerates genetic analysis of pathogen populations and circumvents the difficulties associated with obligate plant pathogens. In principle, this strategy can be widely applied to a variety of plant pathogens. Electronic supplementary material The online version of this article (doi:10.1186/s13059-015-0590-8) contains supplementary material, which is available to authorized users.

Wheat yellow (stripe) rust, caused by the obligate biotrophic fungus Puccinia striiformis f. sp. tritici, is a continual threat to wheat fields worldwide. New isolates with increased virulence have recently emerged driving breeding efforts to incorporate disease resistance genes which confer potentially more durable, albeit partial, resistance. Yr36 is one such locus which was recently cloned (WKS1) and described as a high-temperature adult-plant gene being effective only at temperatures above 25°C. We examined the potential use of Yr36 at temperatures below 25°C. Field experiments in the United Kingdom across 2 years show that lines carrying Yr36 provide slow rusting resistance to the yellow rust pathogen. Juvenile and adult Yr36 isogenic lines showed partial resistance at temperatures below 18°C under control environment conditions in tetraploid and hexaploid genetic backgrounds, but not at seedling stage, when inoculated with U.K. P. striiformis isolates. This partial resistance phenotype was similar to that observed previously at temperatures ≥25°C. Transgenic complementation tests and ethyl methanesulfonate mutants showed that the low-temperature partial resistance was due to the WKS1 gene. This study indicates that Yr36 has the potential to be an effective source of partial resistance in temperate wheat growing regions.

Recent disease outbreaks caused by (re-)emerging plant pathogens have been associated with expansions in pathogen geographic distribution and increased virulence. For example, in the past two decades’ wheat yellow (stripe) rust, Puccinia striiformis f. sp. tritici, has seen the emergence of new races that are adapted to warmer temperatures, have expanded virulence profiles, and are more aggressive than previous races, leading to wide-scale epidemics. Here, we used field-based genotyping to generate high-resolution data on P. striiformis genetics and carried out global population analysis. We also undertook comparative analysis of the 2014 and 2013 UK populations and assessed the temporal dynamics and host specificity of distinct pathogen genotypes. Our analysis revealed that P. striiformis lineages recently detected in Europe are extremely diverse and in fact similar to globally dispersed populations. In addition, we identified a considerable shift in the UK P. striiformis population structure including the first identification of one infamous race known as Kranich. Next, by establishing the genotype of both the pathogen and host within a single infected field sample, we uncovered evidence for varietal specificity for genetic groups of P. striiformis. Finally, we found potential seasonal specificity for certain genotypes of the pathogen with several lineages identified only in samples collected in late spring and into the summer, whereas one lineage was identified throughout the wheat growing season. Our discovery of which wheat varieties are susceptible to which specific P. striiformis isolates, and when those isolates are prevalent throughout the year, represents a powerful tool for disease management.