Wheat Stem Rust Back in Europe: Diversity, Prevalence and Impact on Host Resistance

The objective of this study was to investigate the re-emergence of a previously important crop pathogen in Europe, Puccinia graminis f.sp. tritici, causing wheat stem rust. The pathogen has been insignificant in Europe for more than 60 years, but since 2016 it has caused epidemics on both durum wheat and bread wheat in local areas in southern Europe, and additional outbreaks in Central- and West Europe. The prevalence of three distinct genotypes/races in many areas, Clade III-B (TTRTF), Clade IV-B (TKTTF) and Clade IV-F (TKKTF), suggested clonal reproduction and evolution by mutation within these. None of these genetic groups and races, which likely originated from exotic incursions, were detected in Europe prior to 2016. A fourth genetic group, Clade VIII, detected in Germany (2013), was observed in several years in Central- and East Europe. Tests of representative European wheat varieties with prevalent races revealed high level of susceptibility. In contrast, high diversity with respect to virulence and Simple Sequence Repeat (SSR) markers were detected in local populations on cereals and grasses in proximity to Berberis species in Spain and Sweden, indicating that the alternate host may return as functional component of the epidemiology of wheat stem rust in Europe. A geographically distant population from Omsk and Novosibirsk in western Siberia (Russia) also revealed high genetic diversity, but clearly different from current European populations. The presence of Sr31-virulence in multiple and highly diverse races in local populations in Spain and Siberia stress that virulence may emerge independently when large geographical areas and time spans are considered and that Sr31-virulence is not unique to Ug99. All isolates of the Spanish populations, collected from wheat, rye and grass species, were succesfully recovered on wheat, which underline the plasticity of host barriers within P. graminis. The study demonstrated successful alignment of two genotyping approaches and race phenotyping methodologies employed by different laboratories, which also allowed us to line up with previous European and international studies of wheat stem rust. Our results suggest new initiatives within disease surveillance, epidemiological research and resistance breeding to meet current and future challenges by wheat stem rust in Europe and beyond.info:eu-repo/semantics/publishedVersio

Potential for re-emergence of wheat stem rust in the United Kingdom

Wheat stem rust, a devastating disease of wheat and barley caused by the fungal pathogen Puccinia graminis f. sp. tritici, was largely eradicated in Western Europe during the mid-to-late twentieth century. However, isolated outbreaks have occurred in recent years. Here we investigate whether a lack of resistance in modern European varieties, increased presence of its alternate host barberry and changes in climatic conditions could be facilitating its resurgence. We report the first wheat stem rust occurrence in the United Kingdom in nearly 60 years, with only 20% of UK wheat varieties resistant to this strain. Climate changes over the past 25 years also suggest increasingly conducive conditions for infection. Furthermore, we document the first occurrence in decades of P. graminis on barberry in the UK. Our data illustrate that wheat stem rust does occur in the UK and, when climatic conditions are conducive, could severely harm wheat and barley production.</p

Aegilops sharonensis genome-assisted identification of stem rust resistance gene Sr62

The wild relatives and progenitors of wheat have been widely used as sources of disease resistance (R) genes. Molecular identification and characterization of these R genes facilitates their manipulation and tracking in breeding programmes. Here, we develop a reference-quality genome assembly of the wild diploid wheat relative Aegilops sharonensis and use positional mapping, mutagenesis, RNA-Seq and transgenesis to identify the stem rust resistance gene Sr62, which has also been transferred to common wheat. This gene encodes a tandem kinase, homologues of which exist across multiple taxa in the plant kingdom. Stable Sr62 transgenic wheat lines show high levels of resistance against diverse isolates of the stem rust pathogen, highlighting the utility of Sr62 for deployment as part of a polygenic stack to maximize the durability of stem rust resistance

Recombination in the wheat stem rust pathogen mediated by an indigenous barberry species in Spain

The comeback of wheat stem rust in Europe, caused by Puccinia graminis f. sp. tritici, and the prevalence of the alternate (sexual) host in local areas have recently regained attention as a potential threat to European wheat production. The aim of this study was to investigate a potential epidemiological link between the aecia found on an indigenous barberry species and stem rust infections on nearby cereals and grasses. Aecial infections collected from Berberis vulgaris subsp. seroi were inoculated on a panel of susceptible genotypes of major cereal crop species. In total, 67 stem rust progeny isolates were recovered from wheat (51), barley (7), and rye (9), but none from oat, indicating the potential of barberry derived isolates to infect multiple cereals. Molecular genotyping of the progeny isolates and 20 cereal and grass stem rust samples collected at the same locations and year, revealed a clear genetic relatedness between the progeny isolated from barberry and the stem rust infections found on nearby cereal and grass hosts. Analysis of Molecular Variance indicated that variation between the stem rust populations accounted for only 1%. A Principal Components Analysis using the 62 detected multilocus genotypes also demonstrated a low degree of genetic variation among isolates belonging to the two stem rust populations. Lastly, pairwise comparisons based on fixation index (Fst), Nei’s genetic distances and number of effective migrants (Nm) revealed low genetic differentiation and high genetic exchange between the two populations. Our results demonstrated a direct epidemiological link and functionality of an indigenous barberry species as the sexual host of P. graminis in Spain, a factor that should be considered when designing future strategies to prevent stem rust in Europe and beyond.The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was supported by the Bill and Melinda Gates Foundation and the United Kingdom Department for International Development (Grant Number OPP1133199, Delivering Genetic Gain in Wheat (DGGW), the European Commission, Research and Innovation, Horizon 2020-Sustainable Food Security (Grant number 773311-2, RustWatch), Agencia Estatal de Investigación, Spain (Project PID2020-118650RR-C31).info:eu-repo/semantics/publishedVersio

Recurrent parent genome recovery in the BC₂F₂ generation using 40,584 genome-wide SNPs.

Recurrent parent genome recovery in the BC2F2 generation using 40,584 genome-wide SNPs.</p

Response to stem rust of seedlings from the parental lines used in this study.

Response to stem rust of seedlings from the parental lines used in this study.</p

Physical location of rye chromosome 2R based on GBS data and seedling responses to stem rust races TTTTF and TTKSK.

a) Seedling assay for race TTTTF in the BC2F3 population, where red denotes resistance and green susceptibility; b) physical positions of the 15,116 SNPs from GBS reads in the BC2F2 population, where red denotes the rye allele and dark blue the wheat allele; c) seedling assay for race TTKSK in the BC2F3 population, where red denotes resistance and green susceptibility.</p

PCA plot of rye chromosome 2R using 15,116 SNPs from GBS reads.

A) Resistant parental lines (SLU238, SLU239, and TA5094) with chromosome 2R; B) BC2F2 population comprising recurrent parents carrying chromosome 2RL close to SLU238 and TA5094; C) BC2F2 population derived from recurrent parents carrying the chromosome 2RL segment; D) recurrent parents (BAJ #1, KACHU #1, and REEDLING #1) and the susceptible BC2F2 population without chromosome 2RL; E) lines CSph1bM and CSA.</p

PCA plot of wheat chromosomes using 40,584 SNPs from GBS reads.

Relationship between recurrent parents (BAJ#1, KACHU#1, and REEDLING#1) and lines SLU238, TA5094, CSph1bM, and CSA, based on polymorphic sites in the entire wheat genome as determined by GBS.</p

Crossing, backcrossing, and selection procedures with <i>Pgt</i> race TTTTF, KASP markers, and phenotyping selection in BC₁F₁ and BC₂F₁ populations.

Crossing, backcrossing, and selection procedures with Pgt race TTTTF, KASP markers, and phenotyping selection in BC1F1 and BC2F1 populations.</p