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.

ARVALIS Institut du Végétal Boigneville France

Department of Agroecology Aarhus University Slagelse Denmark

Department of Agronomy Omsk State Agrarian University Omsk Russia

Department of Forest Mycology and Plant Pathology Swedish University of Agricultural Science Uppsala Sweden

Department of Genetics and Plant Breeding Methods Crop Research Institute Prague Czechia

Institute for Food and Agricultural Research and Technology Lleida Spain

Institute of Cytology and Genetics Russian Academy of Sciences Novosibirsk Russia

Julius Kühn Institut Federal Research Centre for Cultivated Plants Institute for Plant Protection in Field Crops and Grassland Quedlinburg Germany

National Agricultural and Food Centre Nitra Slovakia

Plant Breeding and Acclimatization Institute National Research Institute Radzików Poland

Società Semplice Agricola Randazzo Palermo Italy

Université Paris Saclay INRAE UR BIOGER Thiverval Grignon France

USDA ARS Cereal Disease Laboratory University of Minnesota Minneapolis MN United States

Zobrazit více v PubMed

Agapow P. M., Burt A. (2001). Indices of multilocus linkage disequilibrium. Mol. Ecol. Notes 1, 101–102. doi: 10.1046/j.1471-8278.2000.00014.x DOI

Ali S., Gladieux P., Leconte M., Gautier A., Justesen A. F., Hovmoller M. S., et al. (2014). Origin, migration routes and worldwide population genetic structure of the wheat yellow rust pathogen PubMed DOI PMC

Anikster Y. (1985). “The Formae Speciales” in The Cereal Rusts. eds. Roelfs A. P., Bushnell W. R. (New York: Academic Press, Inc.), 115–130.

Bartoš P., Stuchlíková E., Hanušová R. (1996). Adaptation of wheat rusts to the wheat cultivars in former Czechoslovakia. Euphytica 92, 95–103. doi: 10.1007/bf00022834 DOI

Berlin A., Djurle A., Samils B., Yuen J. (2012). Genetic variation in PubMed DOI

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

Brown J. K. M., Hovmøller M. S. (2002). Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297, 537–541. doi: 10.1126/science.1072678, PMID: PubMed DOI

Chen W., Zhang Z., Ma X., Zhang G., Yao Q., Kang Z., et al. (2021). Phenotyping and genotyping analyses reveal the spread of Puccinia striiformis f. sp. PubMed DOI PMC

Groth J. V., Roelfs A. P. (1982). Effect of sexual and asexual reproduction on race abundance in cereal rust fungus populations. Phytopathology 72, 1503–1507. doi: 10.1094/Phyto-72-1503 DOI

Hermansen J. E. (1968). Studies on the spread and survival of cereal rust and mildew diseases in Denmark. Friesia 8, 1–206.

Hovmøller M. S., Sørensen C. K., Walter S., Justesen A. F. (2011). Diversity of Puccinia striiformis on cereals and grasses. Annu. Rev. Phytopathol. 49, 197–217. doi: 10.1146/annurev-phyto-072910-095230 PubMed DOI

Hovmøller M. S., Walter S., Bayles R. A., Hubbard A., Flath K., Sommerfeldt N., et al. (2016). Replacement of the European wheat yellow rust population by new races from the Centre of diversity in the near-Himalayan region. Plant Pathol. 65, 402–411. doi: 10.1111/ppa.12433 DOI

Jin Y., Szabo L. J., Pretorius Z. A., Singh R. P., Ward R., Fetch T. (2008). Detection of virulence to resistance gene Sr24 Within race TTKS of PubMed DOI

Jin Y., Szabo L. J., Rouse M. N., Fetch T., Pretorius Z. A., Wanyera R., et al. (2009). Detection of virulence to resistance gene Sr36 Within the TTKS race lineage of PubMed DOI

Jombart T. (2008). Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405. doi: 10.1093/bioinformatics/btn129, PMID: PubMed DOI

Jombart T., Devillard S., Balloux F. (2010). Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 11:94. doi: 10.1186/1471-2156-11-94, PMID: PubMed DOI PMC

Kamvar Z. N., Brooks J. C., Grünwald N. J. (2015). Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality front. Genet. 6:208. doi: 10.3389/fgene.2015.00208, PMID: PubMed DOI PMC

Kamvar Z. N., Tabima J. F., Grunwald N. J. (2014). Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281. doi: 10.7717/peerj.281, PMID: PubMed DOI PMC

Kjellström C. (2021). Population structure of

Lewis C. M., Persoons A., Bebber D. P., Kigathi R. N., Maintz J., Findlay K., et al. (2018). Potential for re-emergence of wheat stem rust in the United Kingdom. Commun. Biol. 1:13. doi: 10.1038/s42003-018-0013-y, PMID: PubMed DOI PMC

Lind J. (1915). Berberisbusken og Berberisloven. Tidsskrift for Planteavl 22, 729–780.

Luo M., Xie L., Chakraborty S., Wang A., Matny O., Jugovich M., et al. (2021). A five-transgene cassette confers broad-spectrum resistance to a fungal rust pathogen in wheat. Nat. Biotechnol. 39, 561–566. doi: 10.1038/s41587-020-00770-x, PMID: PubMed DOI

Massenot M. (1978). Changes in the race composition of

McIntosh R. A., Hart G. E., Gale M. D. (1995). "Catalogue of wheat symbols for wheat," in

McIntosh R. A., Pretorius Z. A. (2011). Borlaug global rust initiative provides momentum for wheat rust research. Euphytica 179, 1–2. doi: 10.1007/s10681-011-0389-y DOI

Olivera Firpo P. D., Newcomb M., Flath K., Sommerfeldt-Impe N., Szabo L. J., Carter M., et al. (2017). Characterization of DOI

Olivera P., Newcomb M., Szabo L. J., Rouse M., Johnson J., Gale S., et al. (2015). Phenotypic and genotypic characterization of race TKTTF of PubMed DOI

Olivera P. D., Sikharulidze Z., Dumbadze R., Szabo L. J., Newcomb M., Natsarishvili K., et al. (2019). Presence of a Sexual Population of PubMed DOI

Olivera P. D., Villegas D., Cantero-Martínez C., Szabo L. J., Rouse M. N., Luster D. G., et al. (2022). A unique race of the wheat stem rust pathogen with virulence on Sr31 identified in Spain and reaction of wheat and durum cultivars to this race. Plant pathol. 71, 873–889. doi: 10.1111/ppa.13530 DOI

Patpour M., Hovmoller M., Justesen A. F., Newcomb M., Olivera Firpo P. D., Jin Y., et al. (2015). Emergence of virulence to SrTmp in the Ug99 race group of wheat stem rust, DOI

Patpour M., Justesen A. F., Tecle A. W., Yazdani M., Yasaie M., Hovmøller M. S. (2020). First report of race TTRTF of wheat stem rust ( DOI

Peakall R., Smouse P. E. (2012). GenAlEx 6.5: genetic analysis in excel. Population genetic software for teaching and research--an update. Bioinformatics 28, 2537–2539. doi: 10.1093/bioinformatics/bts460, PMID: PubMed DOI PMC

Pretorius Z. A., Singh R. P., Wagoire W. W., Payne T. S. (2000). Detection of virulence to wheat stem rust resistance gene Sr31 in PubMed DOI

Rodriguez-Algaba J., Hovmøller M. S., Villegas D., Cantero-Martínez C., Jin Y., Justesen A. F. (2021). Two indigenous Berberis species From Spain were confirmed as alternate hosts of the yellow rust fungus Puccinia striiformis f. sp. PubMed DOI

Roelfs A. P., Martens J. W. (1984). "Proposal for an International System of Race Nomenclature for Puccinia Graminis f.Sp.

Saunders D. G. O., Pretorius Z. A., Hovmøller M. S. (2019). Tackling the re-emergence of wheat stem rust in Western Europe. Commun. Biol. 2:51. doi: 10.1038/s42003-019-0294-9, PMID: PubMed DOI PMC

Shamanin V., Pototskaya I., Shepelev S., Pozherukova V., Salina E., Skolotneva E., et al. (2020). Stem rust in Western Siberia – race composition and effective resistance genes. Vavilov J. Gene. Breed. 24, 131–138. doi: 10.18699/VJ20.608, PMID: PubMed DOI PMC

Shamanin V., Salina E., Wanyera R., Zelenskiy Y., Olivera P., Morgounov A. (2016). Genetic diversity of spring wheat from Kazakhstan and Russia for resistance to stem rust Ug99. Euphytica 212, 287–296. doi: 10.1007/s10681-016-1769-0 DOI

Shannon C. E. (2001). A mathematical theory of communication. Mob. Comput. Commun. 5, 3–55. doi: 10.1145/584091.584093 DOI

Singh R. P., Hodson D. P., Huerta-Espino J., Jin Y., Bhavani S., Njau P., et al. (2011). The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu. Rev. Phytopathol. 49, 465–481. doi: 10.1146/annurev-phyto-072910-095423, PMID: PubMed DOI

Singh R. P., Hodson D. P., Jin Y., Lagudah E. S., Ayliffe M. A., Bhavani S., et al. (2015). Emergence and spread of new races of wheat stem rust fungus: continued threat to food security and prospects of genetic control. Phytopathology 105, 872–884. doi: 10.1094/phyto-01-15-0030-fi, PMID: PubMed DOI

Stakman E. C. (1923). "Barberry eradication prevents black rust in Western Europe", in Washington: United States Department of Agriculture, Department, Circular.

Stakman E. C., Stewart D. M., Loegering W. Q. (1962). "Identification of physiologic races of Puccinia graminis var. tritici". (Washington D.C.: United States Department of Agriculture Research Service; ).

Stoxen S. (2012). Population Structure of Puccinia Graminis f. sp.

Szabo L., Olivera Firpo P. D., Wanyera R., Visser B., Jin Y. (2022). Development of a diagnostic assay for differentiation between genetic groups in clades I, II, III and IV of PubMed DOI

Thach T., Ali S., de Vallavieille-Pope C., Justesen A. F., Hovmøller M. S. (2016). Worldwide population structure of the wheat rust fungus Puccinia striiformis in the past. Fungal Genet. Biol. 87, 1–8. doi: 10.1016/j.fgb.2015.12.014, PMID: PubMed DOI

Tsushima A., Lewis C. M., Flath K., Kildea S., Saunders D. G. O. (2022). Wheat stem rust recorded for the first time in decades in Ireland. Plant Pathol. 71, 890–900. doi: 10.1111/ppa.13532 PubMed DOI PMC

Walter S., Ali S., Kemen E., Nazari K., Bahri B., Enjalbert J., et al. (2016). Molecular markers for tracking the origin and worldwide distribution of invasive strains of PubMed DOI PMC

Wellings C. R., McIntosh R. A. (1990). Puccinia striiformis f.sp. DOI

Wulff B. B. H., Krattinger S. G. (2022). The long road to engineering durable disease resistance in wheat. Curr. Opin. Biotechnol. 73, 270–275. doi: 10.1016/j.copbio.2021.09.002, PMID: PubMed DOI

Zhong S., Leng Y., Friesen T. L., Faris J. D., Szabo L. J. (2009). Development and characterization of expressed sequence tag-derived microsatellite markers for the wheat stem rust fungus PubMed DOI

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