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.

Aarhus University Flakkebjerg 4200 Denmark

Campo Experimental Valle de México INIFAP Texcoco C P 56237 Mexico

CIMMYT Apdo Postal 6 641 D F México 06600 Mexico

CIMMYT Pakistan Islamabad 44000 Pakistan

Crop Disease Research Program National Agriculture Research Center Islamabad 44000 Pakistan

Crop Research Institute Ruzyně 161 06 Praha 6 Czech Republic

Department of Forest Mycology and Plant Pathology Swedish University of Agricultural Sciences Uppsala 750 07 Sweden

Faculty of Agriculture Department of Plant Breeding and Biotechnology University of Tabriz Tabriz 5166616471 Iran

Instituto Nacional de Investigación Agropecuaria La Estanzuela Mailbox 39173 Colonia Uruguay

International Maize and Wheat Improvement Center 5689 Addis Ababa Ethiopia

John Innes Centre Norwich Research Park Norwich NR4 7UH UK

Limagrain UK Ltd Woolpit IP30 9UP UK

National Institute of Agricultural Botany Cambridge CB3 0LE UK

Pwani University 195 80108 Kilifi Kenya

Seed and Plant Improvement Institute Agricultural Research Education and Extension Organization 4119 Karaj Iran

Tel Aviv University Tel Aviv 69978 Israel

University of Exeter Exeter EX4 4QD UK

University of Minnesota St Paul 55455 MN USA

University of the Free State Bloemfontein 9301 South Africa

Wageningen University Wageningen 6700 The Netherlands

Zobrazit více v PubMed

Olivera Firpo, P. D. et al. Characterization of Puccinia graminis f. sp. tritici isolates derived from an unusual wheat stem rust outbreak in Germany in 2013. Plant Pathol.10.1111/ppa.12674 (2017).

Bhattacharya S. Deadly new wheat disease threatens Europe’s crops. Nature. 2017;542:145–146. doi: 10.1038/nature.2017.21424. PubMed DOI

Peterson, P. D. Stem rust of wheat: from ancient enemy to modern foe. Am. Phytopathol.Soc. (APS Press, St. Paul, 2001).

Singh RP, et al. The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu. Rev. Phytopathol. 2011;49:465–481. doi: 10.1146/annurev-phyto-072910-095423. PubMed DOI

Roelfs, A. P. in The Cereal Rusts. Vol. II (eds A. P. Roelfs & W. R. Bushnell) Ch. Wheat and Rye Stem Rust (Academic Press, Inc., Orlando, Florida, 1985).

Zhao J, Wang M, Chen X, Kang Z. Role of alternate hosts in epidemiology and pathogen variation of cereal rusts. Annu. Rev. Phytopathol. 2016;54:207–228. doi: 10.1146/annurev-phyto-080615-095851. PubMed DOI

Smith K, et al. US preparations for potential introduction of Ug99 strains of wheat stem rust. Outlooks Pest Manag. 2009;20:148–152. doi: 10.1564/20aug02. DOI

Stakman, E. C. Barberry Eradication Prevents Black Rust in Western Europe. (United States Department of Agriculture, Washington D.C., 1923).

Hessayon, D. G. The Cereal Disease Expert. 1st edn, 32 (TBS The Book Service Ltd, UK, 1982).

Berlin, A. Stem rust attacks in Sweden heralds the return of a previously vanquished foe. https://www.slu.se/en/ew-news/2017/11/stem-rust-attacks-in-sweden-heralds-the-return-of-a-previously-vanquished-foe/ (2017).

Duplessis S, et al. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc. Natl Acad. Sci. USA. 2011;108:9166–9171. doi: 10.1073/pnas.1019315108. PubMed DOI PMC

Olivera P, et al. Phenotypic and genotypic characterization of race TKTTF of Puccinia graminis f. sp. tritici that caused a wheat stem rust epidemic in southern Ethiopia in 2013-14. Phytopathology. 2015;105:917–928. doi: 10.1094/PHYTO-11-14-0302-FI. PubMed DOI

Hovmoller, M. S. Global Rust Reference Centre. http://wheatrust.org/ (2017).

Hogg, W. H., Hounam, C. E., Mallik, A. K. & Zadoks, J. C. Meterological Factors Affecting the Epidemiology of Wheat Rusts (World Meteorological Organization, Geneva, 1969).

Agriculture and Horticulture Development Board Recommended Lists. https://cereals.ahdb.org.uk/varieties/ahdb-recommended-lists.aspx (2017).

Waring P. Successes in conserving the Barberry Carpet moth Pareulype berberata (D. & S.) (Geometridae) in England. J. Insect Conserv. 2004;8:167–171. doi: 10.1007/s10841-004-1341-4. DOI

Berlin, A. PopulationBiology of Puccinia graminis (Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences, Uppsala, Sweden, 2012).

Berlin A, Kyaschenko J, Justesen AF, Yuen J. Rust fungi forming aecia on Berberis spp. in Sweden. Plant Dis. 2013;97:1281–1287. doi: 10.1094/PDIS-10-12-0989-RE. PubMed DOI

Singh, R. P., Huerta-Espino, J. H. & Roelfs, A. P. in Bread Wheat: Improvement and Production (Food & Agriculture Organization of the UN, Rome, 2002).

Pretorius ZA, Bender CM, Visser B. The rusts of wild rye in South Africa. S Afr. J. Bot. 2015;96:94–98. doi: 10.1016/j.sajb.2014.10.005. DOI

Uauy C, Wulff BBH, Dubcovsky J. Combining traditional mutagenesis with new high-throughput sequencing and genome editing to reveal hidden variation in polyploid wheat. Annu. Rev. Genet. 2017;51:435–454. doi: 10.1146/annurev-genet-120116-024533. PubMed DOI

Steffenson BJ, et al. Vulnerability of barley to African pathotypes of Puccinia graminis f. sp. tritici and sources of resistance. Phytopathology. 2017;107:950–962. doi: 10.1094/PHYTO-11-16-0400-R. PubMed DOI

Roelfs, A. P. Effects of barberry eradication on stem rust in the United States. Plant Dis. 66, 177–181 (1982).

Berlin A, et al. Disease development and genotypic diversity of Puccinia graminis f. sp. avenae in Swedish oat fields. Plant Pathol. 2013;62:32–40. doi: 10.1111/j.1365-3059.2012.02609.x. DOI

Rodriguez-Algaba J, Walter S, Sorensen CK, Hovmoller MS, Justesen AF. Sexual structures and recombination of the wheat rust fungus Puccinia striiformis on Berberis vulgaris. Fungal Genet. Biol. 2014;70:77–85. doi: 10.1016/j.fgb.2014.07.005. PubMed DOI

Kobayashi S, et al. The JRA-55 reanalysis: general specifications and basic characteristics. J. Meteorol. Soc. Jpn. 2015;93:5–48. doi: 10.2151/jmsj.2015-001. DOI

Burrage SW. Environmental factors influencing the infection of wheat by Puccinia graminis. Ann. Appl. Biol. 1970;66:429–440. doi: 10.1111/j.1744-7348.1970.tb04622.x. DOI

Sillmann J, Kharin VV, Zhang X, Zwiers FW, Bronaugh D. Climate extremes indices in the CMIP5 multimodel ensemble: Part 1. Model evaluation in the present climate. J. Geophys. Res. Atmos. 2013;118:1716–1733. doi: 10.1002/jgrd.50203. DOI

Rouse, M. & Jin, Y. in Abstract 12th International Cereal Rusts Powdery Mildew Conference (ed. Akkaya M. S.) (Antalya, Turkey, 2009).

Hovmoller MS, Walter S, Justesen AF. Escalating threat of wheat rusts. Science. 2010;329:369. doi: 10.1126/science.1194925. PubMed DOI

Li H, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078–2079. doi: 10.1093/bioinformatics/btp352. PubMed DOI PMC

Cingolani P, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strainw1118; iso-2; iso-3. Fly. 2012;6:80–92. doi: 10.4161/fly.19695. PubMed DOI PMC

Chen XM, Line RF, Leung H. Relationship between virulence variation and DNA polymorphism in Puccinia striiformis. Phytopathology. 1993;83:1489–1497. doi: 10.1094/Phyto-83-1489. DOI

Hubbard A, et al. Field pathogenomics reveals the emergence of a diverse wheat yellow rust population. Genome Biol. 2015;16:23. doi: 10.1186/s13059-015-0590-8. PubMed DOI PMC

Upadhyaya NM, et al. Comparative genomics of Australian isolates of the wheat stem rust pathogen Puccinia graminis f. sp. tritici reveals extensive polymorphism in candidate effector genes. Front Plant Sci. 2014;5:759. PubMed PMC

Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688–2690. doi: 10.1093/bioinformatics/btl446. PubMed DOI

Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. Mol. Biol. Evol. 2016;33:1870–1874. doi: 10.1093/molbev/msw054. PubMed DOI PMC

Dutech C, Fabreguettes O, Capdevielle X, Robin C. Multiple introductions of divergent genetic lineages in an invasive fungal pathogen, Cryphonectria parasitica, in France. Heredity. 2010;105:220–228. doi: 10.1038/hdy.2009.164. PubMed DOI

Jombart T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24:1403–1405. doi: 10.1093/bioinformatics/btn129. PubMed DOI

Librado P, Rozas J. DnaSPv5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–1452. doi: 10.1093/bioinformatics/btp187. PubMed DOI

Stakman, E. C., Stewart, D. M. & Loegering, W. Q. Identification of Physiologic Races of Puccinia graminis var. tritici (U.S. Department of Agriculture, Agricultural Research Service, Minnesota, USA, 1962).

Barnes CW, Szabo LJ. Detection and identification of four common rust pathogens of cereals and grasses using real-time polymerase chain reaction. Phytopathology. 2007;97:717–727. doi: 10.1094/PHYTO-97-6-0717. PubMed DOI

Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC

Bebber, D. P., Castillo, A. D. & Gurr, S. J. Modelling coffee leaf rust risk in Colombia with climate reanalysis data. Philos. Trans. R Soc. Lond. B Biol. Sci.371, 10.1098/rstb.2015.0458 (2016). PubMed PMC

Yan WK, Hunt LA. An equation for modelling the temperature response of plants using only the cardinal temperatures. Ann. Bot. Lond. 1999;84:607–614. doi: 10.1006/anbo.1999.0955. DOI

Launay M, et al. Climatic indicators for crop infection risk: application to climate change impacts on five major foliar fungal diseases in Northern France. Agr. Ecosyst. Environ. 2014;197:147–158. doi: 10.1016/j.agee.2014.07.020. DOI

Agency, J. M. (ed Computational and Information Systems Laboratory Research Data Archive at the National Center for Atmospheric Research) https://rda.ucar.edu (2013).

Rogelj J, Meinshausen M, Knutti R. Global warming under old and new scenarios using IPCC climate sensitivity range estimates. Nat. Clim. Change. 2012;2:248–253. doi: 10.1038/nclimate1385. DOI

Jones PG, Thornton PK. Generating downscaled weather data from a suite of climate models for agricultural modelling applications. Agr. Syst. 2013;114:1–5. doi: 10.1016/j.agsy.2012.08.002. DOI

Stem rust on barberry species in Europe: Host specificities and genetic diversity

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

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