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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.

Puccinia striiformisf. sp.hordei, the causal agent of barley stripe rust, is a destructive fungal pathogen that significantly affects barley cultivation. A major constraint in breeding resistant cultivars is the lack of mapping information of resistance (R) genes and their introgression into adapted germplasm. A considerable number ofRgenes have been described in barley toP. striiformisf. sp.hordei, but only a few loci have been mapped. Previously, Chen and Line (1999) reported two recessive seedling resistance loci in the Ethiopian landrace HOR 1428. In this study, we map two loci that confer resistance toP. striiformisf. sp.hordeiin HOR 1428, which are located on chromosomes 3H and 5H. Both loci act as additive effect QTLs, each explaining approximately 20% of the phenotypic variation. We backcrossed HOR 1428 to the cv. Manchuria and selected based on markers flanking theRpsHOR128-5Hlocus. Saturation of theRpsHOR1428-5Hlocus with markers in the region found KASP marker K_1_0292 in complete coupling with resistance toP. striiformisf. sp.hordeiand was designatedRps9. Isolation ofRps9and flanking markers will facilitate the deployment of this genetic resource into existing programs forP. striiformisf. sp.hordeiresistance.

Nonhost resistance is often conceptualized as a qualitative separation from host resistance. Classification into these two states is generally facile, as they fail to fully describe the range of states that exist in the transition from host to nonhost. This poses a problem when studying pathosystems that cannot be classified as either host or nonhost due to their intermediate status relative to these two extremes. In this study, we investigate the efficacy of the Poaceae-stripe rust (Puccinia striiformis Westend.) interaction for describing the host-nonhost landscape. First, using barley (Hordeum vulgare L.) and Brachypodium distachyon (L.) P. Beauv. we observed that macroscopic symptoms of chlorosis and leaf browning were associated with hyphal colonization by P. striiformis f. sp. tritici, respectively. This prompted us to adapt a protocol for visualizing fungal structures into a phenotypic assay that estimates the percent of leaf colonized. Use of this assay in intermediate host and intermediate nonhost systems found the frequency of infection decreases with evolutionary divergence from the host species. Similarly, we observed that the pathogen’s ability to complete its life cycle decreased faster than its ability to colonize leaf tissue, with no incidence of pustules observed in the intermediate nonhost system and significantly reduced pustule formation in the intermediate host system as compared to the host system, barley-P. striiformis f. sp. hordei. By leveraging the stripe rust pathosystem in conjunction with macroscopic and microscopic phenotypic assays, we now hope to dissect the genetic architecture of intermediate host and intermediate nonhost resistance using structured populations in barley and B. distachyon.

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.

Key message We uncouple host and nonhost resistance in barley to Puccinia striiformis ff. spp. hordei and tritici . We isolate, fine map, and physically anchor Rps6 to chromosome 7H in barley. Abstract A plant may be considered a nonhost of a pathogen if all known genotypes of a plant species are resistant to all known isolates of a pathogen species. However, if a small number of genotypes are susceptible to some known isolates of a pathogen species this plant may be considered an intermediate host. Barley (Hordeum vulgare) is an intermediate host for Puccinia striiformis f. sp. tritici (Pst), the causal agent of wheat stripe rust. We wanted to understand the genetic architecture underlying resistance to Pst and to determine whether any overlap exists with resistance to the host pathogen, Puccinia striiformis f. sp. hordei (Psh). We mapped Pst resistance to chromosome 7H and show that host and intermediate host resistance is genetically uncoupled. Therefore, we designate this resistance locus Rps6. We used phenotypic and genotypic selection on F2:3 families to isolate Rps6 and fine mapped the locus to a 0.1 cM region. Anchoring of the Rps6 locus to the barley physical map placed the region on a single fingerprinted contig spanning a physical region of 267 kb. Efforts are now underway to sequence the minimal tiling path and to delimit the physical region harboring Rps6. This will facilitate additional marker development and permit identification of candidate genes in the region. Electronic supplementary material The online version of this article (doi:10.1007/s00122-015-2659-x) contains supplementary material, which is available to authorized users.