Resurgence of wheat stem rust infections in western Europe: causes and how to curtail them.

Ten years ago, (black) stem rust - the most damaging of wheat (Triticum aestivum) rusts - re-emerged in western Europe. Disease incidences have since increased in scale and frequency. Here, we investigated the likely underlying causes and used those to propose urgently needed mitigating actions. We report that the first large-scale UK outbreak of the wheat stem rust fungus, Puccinia graminis f. sp. tritici (Pgt), in 2022 may have been caused by timely arrival of airborne urediniospores from southwest Europe. The drive towards later-maturing wheat varieties in the UK may be exacerbating Pgt incidences, which could have disastrous consequences. Indeed, infection assays showed that two UK Pgt isolates from 2022 could infect over 96% of current UK wheat varieties. We determined that the temperature response data in current disease risk simulation models are outdated. Analysis of germination rates for three current UK Pgt isolates showed substantial variation in temperature response functions, suggesting that the accuracy of disease risk simulations would be substantially enhanced by incorporating data from prevailing Pgt isolates. As Pgt incidences continue to accelerate in western Europe, we advocate for urgent action to curtail Pgt losses and help safeguard future wheat production across the region.

First report of Ug99 Wheat Stem Rust caused by Puccinia graminis f. sp. tritici in South Asia.

Since the emergence of Ug99 wheat stem rust in Uganda in 1998 (Pretorius et al. 2000), the threat of movement into South Asia has been a concern due to long-distance dispersal capacity of airborne spores (Brown and Hovmøller 2002; Singh et al. 2008; Meyer et al. 2017). Increased preparedness by comprehensive rust surveillance efforts and development and deployment of resistant cultivars in advance of an incursion into South Asia has been one of the success stories of the Borlaug Global Rust Initiative (Sharma et al. 2013). In November 2023, an off-season rust survey was conducted in Marpha, Gandaki and Bagmati provinces in Nepal. Rust was only observed at two sites, Dangdunge of Dolakha district and Mude of Sindhupalchok district, where spring wheat was grown as fodder crop outside the main cropping season. Rust infected wheat leaves (10-15 leaves per site) were air dried and sealed in envelopes that were shipped under permit to the Global Rust Reference Center, Denmark. Bulk samples of stem rust, Puccinia graminis f.sp. tritici (Pgt), were recovered from both envelopes, and single pustule isolates were raised and multiplied on Morocco and McNair. Meanwhile, specimens of dry leaves were subjected to SSR genotyping according to standard procedures (Patpour et al. 2022). One distinct multi-locus Pgt genotype was observed, identical to and representing 99% of Ug99 isolates within Clade I collected in East Africa between 2012-2022. A Pgt single pustule isolate from each of the sampling sites were inoculated onto 20 internationally agreed stem rust differential lines using standard procedures, and 14 supplementary lines providing additional resolution of pathogen virulence (Patpour et al. 2022). The pathotyping was repeated in two independent experiments, which resulted in the infection type pattern of Pgt race TTKTT (Supplementary Table 1). Additional independent SSR genotype assays of recovered isolates confirmed the prevalent genotype of Clade I (Patpour et al. 2022; Szabo et al. 2022). This first detection of Ug99 race TTKTT in South Asia emphasizes the need for continued coordinated international surveillance efforts and utilization of diverse sources of resistance to control stem rust in wheat. New surveillance efforts in Nepal during February-March 2024 did not reveal additional cases of wheat stem rust. However, more detailed and sustained rust surveillance efforts, assessment of the vulnerability of current wheat crops to Ug99 and other races of stem-, stripe/yellow- and leaf rust, as well as intensified breeding for rust resistance throughout the region is strongly recommended to meet current and future plant health risks.

First report of race TTRTF of the Wheat Stem Rust pathogen Puccinia graminis f. sp. tritici in Sweden.

Wheat (Triticum aestivum L.) stem rust caused by Puccinia graminis f. sp. tritici (Pgt) was generally insignificant in Europe from the 1960s until 2016, where a new race (TTRTF) caused damage on huge areas of durum wheat and bread wheat in Sicily (Bhattacharya, 2017). During the following five years, TTRTF was detected in eight additional countries in south- and central Europe (Patpour et al. 2022). In July 2021, seven wheat stem rust samples collected from spring wheat and one from barley in Svalov (55° 54' 10.8″ N, 13° 6' 54″ E) and Alnarp (55° 39' 39.6″ N, 13° 4' 40.8″ E), Sweden. Both cereal fields had a total disease incidence of 50% or higher. The samples were sent to the Global Rust Reference Center (GRRC, Denmark). Urediniospores of each sample were recovered on two susceptible cultivars, Line E and Morocco, which were used as susceptible controls in all experiments. Single pustular isolates were extracted and race typing was generally repeated two to three times based on Patpour et al. (2022) using 20 North American stem rust differential lines. Seedling infection types (IT) were scored on the first and second leaf 17 days post-inoculation using a 0-4 scale (Stakman et al. 1962; McIntosh et al. 1995). Isolates conferring 'low' ITs (i.e., 0, 0; 1, 1+, 2, and 2+), or combinations thereof, were considered 'avirulent' (incompatible), whereas ITs of 3-, 3, 3+, and 4 were considered 'high' (i.e., compatible, 'virulent'). Race nomenclature was based on a modified letter code proposed by Jin et al. (2008). We conducted DNA extraction and molecular genotyping using seventeen Simple Sequence Repeat (SSR) primer pairs derived from Stoxen (2012) and applied at large scale by Patpour et al. (2022). Based on the results from pathotyping and genotyping, two samples from wheat showed Pgt race TKTTF (Clade IV-B), three from wheat TKKTF (Clade IV- F), and three samples from wheat and barley were identified as TTRTF (Clade III-B). This is the first report of race TTRTF in northern Europe, particularly, Sweden, which significantly extends the known distribution of this race. The TTRTF race is a serious threat to wheat productivity and evaluation of resistance of commercial European wheat varieties to the TTRTF race confirmed that 70% of the cultivars were susceptible (Patpour et al. 2022). Therefore, if the conditions are suitable for the establishment and development of stem rust, the disease can cause significant damage to the wheat crop in these countries. Susceptibility of European wheat varieties stress an urgent need to initiate new breeding efforts to identify effective sources of resistance to wheat stem rust in breeding programs. Funding: The work is funded by the European Union's Horizon 2020 research and innovation programme under grant agreement No 773311 (RustWatch). References: Bhattacharya, S. 2017. Nature 542, 145-146. Doi: 10.1038/nature.2017.21424 Jin, Y., et al. 2008. Plant Dis. 92:923. 10.1094/PDIS-92-6-0923 McIntosh, R. A. et al. 1995. Catalogue of wheat symbols for wheat. 1993, Beijing, China, 1333-1451. Patpour, M., et al. 2022. Front. Plant Sci., 02 June 2022 | https://doi.org/10.3389/fpls.2022.882440. Stakman, E. C., et al. 1962. ARS E-617. USDA, Washington, DC. USA. Stoxen, S. 2012. Master's Thesis, University of Minnesota, Minneapolis, MN USA.

Emergence and Spread of New Races of Wheat Stem Rust Fungus: Continued Threat to Food Security and Prospects of Genetic Control.

Race Ug99 (TTKSK) of Puccinia graminis f. sp. tritici, detected in Uganda in 1998, has been recognized as a serious threat to food security because it possesses combined virulence to a large number of resistance genes found in current widely grown wheat (Triticum aestivum) varieties and germplasm, leading to its potential for rapid spread and evolution. Since its initial detection, variants of the Ug99 lineage of stem rust have been discovered in Eastern and Southern African countries, Yemen, Iran, and Egypt. To date, eight races belonging to the Ug99 lineage are known. Increased pathogen monitoring activities have led to the identification of other races in Africa and Asia with additional virulence to commercially important resistance genes. This has led to localized but severe stem rust epidemics becoming common once again in East Africa due to the breakdown of race-specific resistance gene SrTmp, which was deployed recently in the 'Digalu' and 'Robin' varieties in Ethiopia and Kenya, respectively. Enhanced research in the last decade under the umbrella of the Borlaug Global Rust Initiative has identified various race-specific resistance genes that can be utilized, preferably in combinations, to develop resistant varieties. Research and development of improved wheat germplasm with complex adult plant resistance (APR) based on multiple slow-rusting genes has also progressed. Once only the Sr2 gene was known to confer slow rusting APR; now, four more genes-Sr55, Sr56, Sr57, and Sr58-have been characterized and additional quantitative trait loci identified. Cloning of some rust resistance genes opens new perspectives on rust control in the future through the development of multiple resistance gene cassettes. However, at present, disease-surveillance-based chemical control, large-scale deployment of new varieties with multiple race-specific genes or adequate levels of APR, and reducing the cultivation of susceptible varieties in rust hot-spot areas remains the best stem rust management strategy.

Development and Validation of a Mechanistic, Weather-Based Model for Predicting Puccinia graminis f. sp. tritici Infections and Stem Rust Progress in Wheat.

Stem rust (or black rust) of wheat, caused by Puccinia graminis f. sp. tritici (Pgt), is a re-emerging, major threat to wheat production worldwide. Here, we retrieved, analyzed, and synthetized the available information about Pgt to develop a mechanistic, weather-driven model for predicting stem rust epidemics caused by uredospores. The ability of the model to predict the first infections in a season was evaluated using field data collected in three wheat-growing areas of Italy (Emilia-Romagna, Apulia, and Sardinia) from 2016 to 2021. The model showed good accuracy, with a posterior probability to correctly predict infections of 0.78 and a probability that there was no infection when not predicted of 0.96. The model's ability to predict disease progress during the growing season was also evaluated by using published data obtained from trials in Minnesota, United States, in 1968, 1978, and 1979, and in Pennsylvania, United States, in 1986. Comparison of observed versus predicted data generated a concordance correlation coefficient of 0.96 and an average distance between real data and the fitted line of 0.09. The model could therefore be considered accurate and reliable for predicting epidemics of wheat stem rust and could be tested for its ability to support risk-based control of the disease.

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.