Agricultural diseases are a major threat to sustainable food production. Yet, for many pathogens we know exceptionally little about their epidemiological and population dynamics, and this knowledge gap is slowing the development of efficient control strategies. Here we study the population genomics and molecular epidemiology of wheat powdery mildew, a disease caused by the biotrophic fungus Blumeria graminis forma specialis tritici (Bgt). We sampled Bgt across two consecutive years, 2022 and 2023, and compiled a genomic dataset of 415 Bgt isolates from 22 countries in Europe and surrounding regions. We identified a single epidemic unit in the north of Europe, consisting of a highly homogeneous population. Conversely, the south of Europe hosts smaller local populations which are less interconnected. In addition, we show that the population structure can be largely predicted by the prevalent wind patterns. We identified several loci that were under selection in the recent past, including fungicide targets and avirulence genes. Some of these loci are common between populations, while others are not, suggesting different local selective pressures. We reconstructed the evolutionary history of one of these loci, AvrPm17, coding for an effector recognized by the wheat receptor Pm17. We found evidence for a soft sweep on standing genetic variation. Multiple AvrPm17 haplotypes, which can partially escape recognition by Pm17, spread rapidly throughout the continent upon its introduction in the early 2000s. We also identified a new virulent variant, which emerged more recently and can evade Pm17 resistance altogether. Overall, we highlight the potential of genomic surveillance in resolving the evolutionary and epidemiological dynamics of agricultural pathogens, as well as in guiding control strategies.

Agricultural Institute HUN REN Centre for Agricultural Research Martonvásár Hungary

Agriculture Faculty University of Life Sciences King Mihai 1 from Timișoara Timișoara Romania

Agroscope Department of Plant Breeding Nyon Switzerland

Arvalis Institut du végétal Station Expérimentale Boigneville France

Centro de Biotecnología y Genómica de Plantas Universidad Politécnica de Madrid Madrid Spain

Centro Ricerche e Sperimentazione per il Miglioramento Vegetale N Strampelli Macerata Italy

CIMMYT Turkey Ankara Turkey

Council for Agricultural Research and Economics Research Centre for Genomics and Bioinformatics Fiorenzuola d'Arda Italy

Department of Agricultural and Food Sciences University of Bologna Bologna Italy

Department of Agricultural Sciences University of Sassari Sassari Italy

Department of Agriculture Aristotle University of Thessaloniki Thessaloniki Greece

Department of Agronomy University of Seville Seville Spain

Department of Genetics Genomics and Cancer Science University of Leicester Leicester United Kingdom

Department of Integrated Plant Protection Agrotest Fyto Ltd Kroměříž Czech Republic

Department of Microbiology and Genetics Spanish Portuguese Institute for Agricultural Research University of Salamanca Salamanca Spain

Department of Plant and Microbial Biology University of Zurich Zurich Switzerland

Department of Plant Biology Swedish University of Agricultural Sciences Uppsala Sweden

Department of Soil Plant and Food Sciences University of Bari Aldo Moro Bari Italy

Department of Vegetable and Field Crops Institute of Plant Sciences Agricultural Research Organization Volcani Institute Rishon LeZion Israel

Deutsche Saatveredelung AG Leutewitz Germany

Estacion Experimental de Aula Dei CSIC Zaragoza Spain

Haute école des sciences agronomiques forestières et alimentaires Bern Switzerland

Hungarian Research Institute of Organic Agriculture Budapest Hungary

Institut für Pflanzenschutz in Ackerbau und Grünland Julius Kühn Institut Bundesforschungsinstitut für Kulturpflanzen Braunschweig Germany

Institute for Life and Earth Sciences School of Energy Geosciences Infrastructure and Society Heriot Watt University Edinburgh United Kingdom

Institute of Agriculture Lithuanian Research Centre for Agriculture and Forestry Akademija Lithuania

Institute of Genetics Breeding and Biotechnology of Plants University of Life Sciences in Lublin Lublin Poland

Latvia University of Life sciences and technologies Jelgava Latvia

NIAB Cambridge Crop Research Cambridge United Kingdom

Plant Breeding and Acclimatization Institute National Research Institute Radzików Poland

School of Agriculture and Food Science University College Dublin Belfield Dublin Ireland

State Plant Breeding Institute University of Hohenheim Stuttgart Germany

Sustainable Field Crops IRTA Lleida Spain

Teagasc Crops Research Oak Park Carlow Ireland

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Zobrazit více v PubMed

Köser CU, Ellington MJ, Cartwright EJP, Gillespie SH, Brown NM, Farrington M, et al.. Routine use of microbial whole genome sequencing in diagnostic and public health microbiology. PLoS Pathog. 2012;8(8):e1002824. doi: 10.1371/journal.ppat.1002824 . PubMed DOI PMC

Gardy JL, Loman NJ. Towards a genomics-informed, real-time, global pathogen surveillance system. Nat Rev Genet. 2018;19(1):9–20. doi: 10.1038/nrg.2017.88 . PubMed DOI PMC

Baker KS, Jauneikaite E, Hopkins KL, Lo SW, Sánchez-Busó L, Getino M, et al.. Genomics for public health and international surveillance of antimicrobial resistance. Lancet Microb. 2023;4(12):e1047–55. doi: 10.1016/S2666-5247(23)00283-5 . PubMed DOI

Robishaw JD, Alter SM, Solano JJ, Shih RD, DeMets DL, Maki DG, et al.. Genomic surveillance to combat COVID-19: challenges and opportunities. Lancet Microb. 2021;2(9):e481–4. doi: 10.1016/S2666-5247(21)00121-X . PubMed DOI PMC

Cardona-Ospina JA, Rojas-Gallardo DM, Garzón-Castaño SC, Jiménez-Posada EV, Rodríguez-Morales AJ. Phylodynamic analysis in the understanding of the current COVID-19 pandemic and its utility in vaccine and antiviral design and assessment. Hum Vacc Immunother. 2021;17(8):2437–44. doi: 10.1080/21645515.2021.1880254 . PubMed DOI PMC

Attwood SW, Hill SC, Aanensen DM, Connor TR, Pybus OG. Phylogenetic and phylodynamic approaches to understanding and combating the early SARS-CoV-2 pandemic. Nat Rev Genet. 2022;23(9):547–62. doi: 10.1038/s41576-022-00483-8 . PubMed DOI PMC

Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N, Nelson A. The global burden of pathogens and pests on major food crops. Nat Ecol Evol. 2019;3(3):430–9. doi: 10.1038/s41559-018-0793-y . PubMed DOI

McDonald BA, McDermott JM. Population genetics of plant pathogenic fungi: electrophoretic markers give unprecedented precision to analyses of genetic structure of populations. BioScience. 1993;43(5):311–9. doi: 10.2307/1312063 DOI

McDonald BA, Linde C. Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol. 2002;40:349–79. doi: 10.1146/annurev.phyto.40.120501.101443 . PubMed DOI

Milgroom MG, Peever TL. Population biology of plant pathogens: the synthesis of plant disease epidemiology and population genetics. Plant Dis. 2003;87(6):608–17. doi: 10.1094/PDIS.2003.87.6.608 . PubMed DOI

Sánchez-Martín J, Keller B. Contribution of recent technological advances to future resistance breeding. Theor Appl Genet. 2019;132(3):713–32. doi: 10.1007/s00122-019-03297-1 . PubMed DOI

Weisberg AJ, Grünwald NJ, Savory EA, Putnam ML, Chang JH. Genomic approaches to plant-pathogen epidemiology and diagnostics. Annu Rev Phytopathol. 2021;59:311–32. doi: 10.1146/annurev-phyto-020620-121736 . PubMed DOI

Minter F, Saunders DG. Safeguarding wheat yields from cereal fungal invaders in the postgenomic era. Curr Opin Microbiol. 2023;73:102310. doi: 10.1016/j.mib.2023.102310 . PubMed DOI

Saponari M, Giampetruzzi A, Loconsole G, Boscia D, Saldarelli P. Xylella fastidiosa in olive in Apulia: Where we stand. Phytopathology. 2019;109(2):175–86. doi: 10.1094/PHYTO-08-18-0319-FI . PubMed DOI

Islam MT, Croll D, Gladieux P, Soanes DM, Persoons A, Bhattacharjee P, et al.. Emergence of wheat blast in Bangladesh was caused by a South American lineage of Magnaporthe oryzae. BMC Biol. 2016;14(1):84. doi: 10.1186/s12915-016-0309-7 . PubMed DOI PMC

Latorre SM, Were VM, Foster AJ, Langner T, Malmgren A, Harant A, et al.. Genomic surveillance uncovers a pandemic clonal lineage of the wheat blast fungus. PLoS Biol. 2023;21(4):e3002052. doi: 10.1371/journal.pbio.3002052 . PubMed DOI PMC

Hubbard A, Lewis CM, Yoshida K, Ramirez-Gonzalez RH, de Vallavieille-Pope C, Thomas J, et al.. Field pathogenomics reveals the emergence of a diverse wheat yellow rust population. Genome Biol. 2015;16(1):23. doi: 10.1186/s13059-015-0590-8 . PubMed DOI PMC

Production: Crops and livestock products. 2023.

Dean R, Van Kan JAL, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, et al.. The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol. 2012;13(4):414–30. doi: 10.1111/j.1364-3703.2011.00783.x . PubMed DOI PMC

Liu M, Braun U, Takamatsu S, Hambleton S, Shoukouhi P, Bisson KR, et al.. Taxonomic revision of Blumeria based on multi-gene DNA sequences, host preferences and morphology. Mycoscience. 2021;62(3):143–65. doi: 10.47371/mycosci.2020.12.003 . PubMed DOI PMC

Cowger C, Miranda L, Griffey C, Hall M, Murphy JP, Maxwell J. Wheat powdery mildew. Disease Resistance in Wheat. 2012:84–119. doi: 10.1079/9781845938185.0084 DOI

Wyand RA, Brown JKM. Sequence variation in the CYP51 gene of Blumeria graminis associated with resistance to sterol demethylase inhibiting fungicides. Fungal Genet Biol. 2005;42(8):726–35. doi: 10.1016/j.fgb.2005.04.007 . PubMed DOI

Arnold C. Molecular evolution of fungicide resistance in Blumeria graminis. n.d. .

Meyers E, Arellano C, Cowger C. Sensitivity of the U.S. Blumeria graminis f. sp. tritici population to demethylation inhibitor fungicides. Plant Dis. 2019;103(12):3108–16. doi: 10.1094/PDIS-04-19-0715-RE . PubMed DOI

Bennett FGA. Resistance to powdery mildew in wheat: a review of its use in agriculture and breeding programmes. Plant Pathol. 1984;33(3):279–300. doi: 10.1111/j.1365-3059.1984.tb01324.x DOI

Müller MC, Kunz L, Schudel S, Lawson AW, Kammerecker S, Isaksson J, et al.. Ancient variation of the AvrPm17 gene in powdery mildew limits the effectiveness of the introgressed rye Pm17 resistance gene in wheat. Proc Natl Acad Sci U S A. 2022;119(30):e2108808119. doi: 10.1073/pnas.2108808119 . PubMed DOI PMC

Kunz L, Sotiropoulos AG, Graf J, Razavi M, Keller B, Müller MC. The broad use of the Pm8 resistance gene in wheat resulted in hypermutation of the AvrPm8 gene in the powdery mildew pathogen. BMC Biol. 2023;21(1):29. doi: 10.1186/s12915-023-01513-5 . PubMed DOI PMC

Wulff BB, Krattinger SG. The long road to engineering durable disease resistance in wheat. Curr Opin Biotechnol. 2022;73:270–5. doi: 10.1016/j.copbio.2021.09.002 . PubMed DOI

Brown JKM. Durable resistance of crops to disease: a Darwinian perspective. Annu Rev Phytopathol. 2015;53:513–39. doi: 10.1146/annurev-phyto-102313-045914 . PubMed DOI

Bourras S, McNally KE, Ben-David R, Parlange F, Roffler S, Praz CR, et al.. Multiple avirulence loci and allele-specific effector recognition control the Pm3 race-specific resistance of wheat to powdery mildew. Plant Cell. 2015;27(10):2991–3012. doi: 10.1105/tpc.15.00171 . PubMed DOI PMC

Praz CR, Bourras S, Zeng F, Sánchez-Martín J, Menardo F, Xue M, et al.. AvrPm2 encodes an RNase-like avirulence effector which is conserved in the two different specialized forms of wheat and rye powdery mildew fungus. New Phytol. 2017;213(3):1301–14. doi: 10.1111/nph.14372 . PubMed DOI PMC

McNally KE, Menardo F, Lüthi L, Praz CR, Müller MC, Kunz L, et al.. Distinct domains of the AVRPM3A2/F2 avirulence protein from wheat powdery mildew are involved in immune receptor recognition and putative effector function. New Phytol. 2018;218(2):681–95. doi: 10.1111/nph.15026 . PubMed DOI PMC

Bourras S, Kunz L, Xue M, Praz CR, Müller MC, Kälin C, et al.. The AvrPm3-Pm3 effector-NLR interactions control both race-specific resistance and host-specificity of cereal mildews on wheat. Nat Commun. 2019;10(1):2292. doi: 10.1038/s41467-019-10274-1 . PubMed DOI PMC

Hewitt T, Müller MC, Molnár I, Mascher M, Holušová K, Šimková H, et al.. A highly differentiated region of wheat chromosome 7AL encodes a Pm1a immune receptor that recognizes its corresponding AvrPm1a effector from Blumeria graminis. New Phytol. 2021;229(5):2812–26. doi: 10.1111/nph.17075 . PubMed DOI PMC

Manser B, Koller T, Praz CR, Roulin AC, Zbinden H, Arora S, et al.. Identification of specificity-defining amino acids of the wheat immune receptor Pm2 and powdery mildew effector AvrPm2. Plant J. 2021;106(4):993–1007. doi: 10.1111/tpj.15214 . PubMed DOI

Kloppe T, Whetten RB, Kim S-B, Powell OR, Lück S, Douchkov D, et al.. Two pathogen loci determine Blumeria graminis f. sp. tritici virulence to wheat resistance gene Pm1a. New Phytol. 2023;238(4):1546–61. doi: 10.1111/nph.18809 PubMed DOI

Kunz L, Jigisha J, Menardo F, Sotiropoulos AG, Zbinden H, Zou S, et al.. Avirulence depletion assay: Combining R gene-mediated selection with bulk sequencing for rapid avirulence gene identification in wheat powdery mildew. PLoS Pathog. 2025;21(1):e1012799. doi: 10.1371/journal.ppat.1012799 PubMed DOI PMC

Manser B, Zbinden H, Herren G, Steger J, Isaksson J, Bräunlich S, et al.. Wheat zinc finger protein TaZF interacts with both the powdery mildew AvrPm2 protein and the corresponding wheat Pm2a immune receptor. Plant Commun. 2024;5(5):100769. doi: 10.1016/j.xplc.2023.100769 . PubMed DOI PMC

Wicker T, Oberhaensli S, Parlange F, Buchmann JP, Shatalina M, Roffler S, et al.. The wheat powdery mildew genome shows the unique evolution of an obligate biotroph. Nat Genet. 2013;45(9):1092–6. doi: 10.1038/ng.2704 . PubMed DOI

Sotiropoulos AG, Arango-Isaza E, Ban T, Barbieri C, Bourras S, Cowger C, et al.. Global genomic analyses of wheat powdery mildew reveal association of pathogen spread with historical human migration and trade. Nat Commun. 2022;13(1):4315. doi: 10.1038/s41467-022-31975-0 . PubMed DOI PMC

Limpert E, Felsenstein FG, Andrivon D. Analysis of virulence in populations of wheat powdery mildew in Europe. J Phytopathol. 1987;120(1):1–8. doi: 10.1111/j.1439-0434.1987.tb04408.x DOI

Hermansen JE, Torp U, Prahm LP. Studies of transport of live spores of cereal mildew and rust fungi across the North Sea. Grana. 1978;17(1):41–6. doi: 10.1080/00173137809428851 DOI

Limpert E. Dispersal of cereal mildews across Europe. Agr Forest Meteorol. 1999;97(4):293–308. doi: 10.1016/s0168-1923(99)00073-8 DOI

Peever TL, Zeigler RS, Dorrance AE, Correa-Victoria FJ. Pathogen population genetics and breeding for disease resistance. APSnet Features. 2000. doi: 10.1094/apsnetfeature-2000-0700 DOI

Menardo F, Praz CR, Wyder S, Ben-David R, Bourras S, Matsumae H, et al.. Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species. Nat Genet. 2016;48(2):201–5. doi: 10.1038/ng.3485 . PubMed DOI

Müller MC, Praz CR, Sotiropoulos AG, Menardo F, Kunz L, Schudel S, et al.. A chromosome-scale genome assembly reveals a highly dynamic effector repertoire of wheat powdery mildew. New Phytol. 2019;221(4):2176–89. doi: 10.1111/nph.15529 . PubMed DOI PMC

Alexander DH, Novembre J, Lange K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 2009;19(9):1655–64. doi: 10.1101/gr.094052.109 . PubMed DOI PMC

Lawson DJ, Hellenthal G, Myers S, Falush D. Inference of population structure using dense haplotype data. PLoS Genet. 2012;8(1):e1002453. doi: 10.1371/journal.pgen.1002453 . PubMed DOI PMC

Bradburd GS, Coop GM, Ralph PL. Inferring continuous and discrete population genetic structure across space. Genetics. 2018;210(1):33–52. doi: 10.1534/genetics.118.301333 . PubMed DOI PMC

Lawson DJ, van Dorp L, Falush D. A tutorial on how not to over-interpret structure and admixture bar plots. Nat Commun. 2018;9(1):3258. doi: 10.1038/s41467-018-05257-7 . PubMed DOI PMC

McDonald BA, Stukenbrock EH. Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security. Philos Trans R Soc Lond B Biol Sci. 2016;371(1709):20160026. doi: 10.1098/rstb.2016.0026 PubMed DOI PMC

Marchi N, Schlichta F, Excoffier L. Demographic inference. Curr Biol. 2021;31(6):R276–9. doi: 10.1016/j.cub.2021.01.053 . PubMed DOI

Tellier A, Lemaire C. Coalescence 2.0: A multiple branching of recent theoretical developments and their applications. Mol Ecol. 2014;23(11):2637–52. doi: 10.1111/mec.12755 . PubMed DOI

Menardo F, Gagneux S, Freund F. Multiple merger genealogies in outbreaks of Mycobacterium tuberculosis. Mol Biol Evol. 2021;38(1):290–306. doi: 10.1093/molbev/msaa179 . PubMed DOI PMC

Korfmann K, Sellinger TPP, Freund F, Fumagalli M, Tellier A. Simultaneous inference of past demography and selection from the ancestral recombination graph under the beta coalescent. Peer Commun J. 2024;4. doi: 10.24072/pcjournal.397 DOI

Freund F, Kerdoncuff E, Matuszewski S, Lapierre M, Hildebrandt M, Jensen JD, et al.. Interpreting the pervasive observation of U-shaped site frequency spectra. PLoS Genet. 2023;19(3):e1010677. doi: 10.1371/journal.pgen.1010677 PubMed DOI PMC

Bradburd GS, Ralph PL. Spatial population genetics: It’s about time. Annu Rev Ecol Evol Syst. 2019;50(1):427–49. doi: 10.1146/annurev-ecolsys-110316-022659 DOI

Petkova D, Novembre J, Stephens M. Visualizing spatial population structure with estimated effective migration surfaces. Nat Genet. 2016;48(1):94–100. doi: 10.1038/ng.3464 . PubMed DOI PMC

Marcus J, Ha W, Barber RF, Novembre J. Fast and flexible estimation of effective migration surfaces. Elife. 2021;10:e61927. doi: 10.7554/eLife.61927 . PubMed DOI PMC

Kling M. Windscape: Landscape connectivity by wind. 2024.

Kling MM, Ackerly DD. Global wind patterns shape genetic differentiation, asymmetric gene flow, and genetic diversity in trees. Proc Natl Acad Sci U S A. 2021;118(17):e2017317118. doi: 10.1073/pnas.2017317118 . PubMed DOI PMC

Henden L, Lee S, Mueller I, Barry A, Bahlo M. Identity-by-descent analyses for measuring population dynamics and selection in recombining pathogens. PLoS Genet. 2018;14(5):e1007279. doi: 10.1371/journal.pgen.1007279 . PubMed DOI PMC

Minadakis N, Jigisha J, Cornetti L, Kunz L, Müller MC, Torriani SFF, et al.. Genomic surveillance and molecular evolution of fungicide resistance in European populations of wheat powdery mildew. Mol Plant Pathol. 2025;26(3): e70071. doi: 10.1111/mpp.70071 PubMed PMC

Mallick B, van den Berg J. Intergenerational grounding of women’s environmental non-migration. Popul Environ. 2025;47(1):7. doi: 10.1007/s11111-025-00475-w . PubMed DOI PMC

Koller T, Brunner S, Herren G, Sanchez-Martin J, Hurni S, Keller B. Field grown transgenic Pm3e wheat lines show powdery mildew resistance and no fitness costs associated with high transgene expression. Transgenic Res. 2019;28(1):9–20. doi: 10.1007/s11248-018-0099-5 . PubMed DOI

Camenzind M, Koller T, Armbruster C, Jung E, Brunner S, Herren G, et al.. Breeding for durable resistance against biotrophic fungal pathogens using transgenes from wheat. Mol Breed. 2024;44(2):8. doi: 10.1007/s11032-024-01451-2 . PubMed DOI PMC

Mühlichen M, Doblhammer G. Social differences in cause-specific infant mortality at the dawn of the demographic transition: New insights from German church records. Popul Environ. 2025;47(1):15. doi: 10.1007/s11111-025-00483-w . PubMed DOI PMC

Liu R, Lu J, Zhou M, Zheng S, Liu Z, Zhang C, et al.. Developing stripe rust resistant wheat (Triticum aestivum L.) lines with gene pyramiding strategy and marker-assisted selection. Genet Resour Crop Evol. 2020;67(2):381–91. doi: 10.1007/s10722-019-00868-5 DOI

Marchal C, Pai H, Kamoun S, Kourelis J. Emerging principles in the design of bioengineered made-to-order plant immune receptors. Curr Opin Plant Biol. 2022;70:102311. doi: 10.1016/j.pbi.2022.102311 . PubMed DOI

Zdrzałek R, Stone C, De la Concepcion JC, Banfield MJ, Bentham AR. Pathways to engineering plant intracellular NLR immune receptors. Curr Opin Plant Biol. 2023;74:102380. doi: 10.1016/j.pbi.2023.102380 . PubMed DOI

Koller T, Camenzind M, Jung E, Brunner S, Herren G, Armbruster C, et al.. Pyramiding of transgenic immune receptors from primary and tertiary wheat gene pools improves powdery mildew resistance in the field. J Exp Bot. 2024;75(7):1872–86. doi: 10.1093/jxb/erad493 . PubMed DOI PMC

Amezrou R, Audéon C, Compain J, Gélisse S, Ducasse A, Saintenac C, et al.. A secreted protease-like protein in Zymoseptoria tritici is responsible for avirulence on Stb9 resistance gene in wheat. PLoS Pathog. 2023;19(5):e1011376. doi: 10.1371/journal.ppat.1011376 . PubMed DOI PMC

Lubega J, Figueroa M, Dodds PN, Kanyuka K. Comparative analysis of the avirulence effectors produced by the fungal stem rust pathogen of wheat. Mol Plant Microb Interact. 2024;37(3):171–8. doi: 10.1094/MPMI-10-23-0169-FI . PubMed DOI

Guo Y, Betzen B, Salcedo A, He F, Bowden RL, Fellers JP, et al.. Population genomics of Puccinia graminis f.sp. tritici highlights the role of admixture in the origin of virulent wheat rust races. Nat Commun. 2022;13(1):6287. doi: 10.1038/s41467-022-34050-w . PubMed DOI PMC

Feurtey A, Lorrain C, McDonald MC, Milgate A, Solomon PS, Warren R, et al.. A thousand-genome panel retraces the global spread and adaptation of a major fungal crop pathogen. Nat Commun. 2023;14(1):1059. doi: 10.1038/s41467-023-36674-y . PubMed DOI PMC

Li Y, Dai J, Zhang T, Wang B, Zhang S, Wang C, et al.. Genomic analysis, trajectory tracking, and field surveys reveal sources and long-distance dispersal routes of wheat stripe rust pathogen in China. Plant Commun. 2023;4(4):100563. doi: 10.1016/j.xplc.2023.100563 . PubMed DOI PMC

d’Andrimont R, Verhegghen A, Lemoine G, Kempeneers P, Meroni M, van der Velde M. From parcel to continental scale – A first European crop type map based on Sentinel-1 and Lucas Copernicus in-situ observations. Remote Sens Environ. 2021;266:112708. doi: 10.1016/j.rse.2021.112708 DOI

Torriani SF, Brunner PC, McDonald BA, Sierotzki H. QoI resistance emerged independently at least 4 times in European populations of Mycosphaerella graminicola. Pest Manag Sci. 2009;65(2):155–62. doi: 10.1002/ps.1662 . PubMed DOI

Schulthess AW, Kale SM, Liu F, Zhao Y, Philipp N, Rembe M, et al.. Genomics-informed prebreeding unlocks the diversity in genebanks for wheat improvement. Nat Genet. 2022;54(10):1544–52. doi: 10.1038/s41588-022-01189-7 . PubMed DOI

Jankovics T, Komáromi J, Fábián A, Jäger K, Vida G, Kiss L. New insights into the life cycle of the wheat powdery mildew: Direct observation of ascosporic infection in Blumeria graminis f. sp. tritici. Phytopathology. 2015;105(6):797–804. doi: 10.1094/PHYTO-10-14-0268-R . PubMed DOI

Hacquard S, Kracher B, Maekawa T, Vernaldi S, Schulze-Lefert P, Ver Loren van Themaat E. Mosaic genome structure of the barley powdery mildew pathogen and conservation of transcriptional programs in divergent hosts. Proc Natl Acad Sci U S A. 2013;110(24):E2219-28. doi: 10.1073/pnas.1306807110 . PubMed DOI PMC

Zhang Z, Henderson C, Perfect E, Carver TLW, Thomas BJ, Skamnioti P, et al.. Of genes and genomes, needles and haystacks: Blumeria graminis and functionality. Mol Plant Pathol. 2005;6(5):561–75. doi: 10.1111/j.1364-3703.2005.00303.x . PubMed DOI

Eldon B. Evolutionary genomics of high fecundity. Annu Rev Genet. 2020;54:213–36. doi: 10.1146/annurev-genet-021920-095932 . PubMed DOI

Hedgecock D, Pudovkin AI. Sweepstakes reproductive success in highly fecund marine fish and shellfish: A review and commentary. BMS. 2011;87(4):971–1002. doi: 10.5343/bms.2010.1051 DOI

Durrett R, Schweinsberg J. A coalescent model for the effect of advantageous mutations on the genealogy of a population. Stochastic Process Appl. 2005;115(10):1628–57. doi: 10.1016/j.spa.2005.04.009 DOI

Árnason E, Koskela J, Halldórsdóttir K, Eldon B. Sweepstakes reproductive success via pervasive and recurrent selective sweeps. Elife. 2023;12:e80781. doi: 10.7554/eLife.80781 . PubMed DOI PMC

Vidal-Villarejo M, Freund F, Hanekamp H, von Tiedemann A, Schmid K. Population genomic evidence for a repeated introduction and rapid expansion of the fungal maize pathogen Setosphaeria turcica in Europe. Genome Biol Evol. 2023;15(8):evad130. doi: 10.1093/gbe/evad130 . PubMed DOI PMC

RODERICK HW, JONES ERL, ŠEBESTA J. Resistance to oat powdery mildew in Britain and Europe: A review. Ann Appl Biol. 2000;136(1):85–91. doi: 10.1111/j.1744-7348.2000.tb00012.x DOI

Rohland N, Reich D. Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture. Genome Res. 2012;22(5):939–46. doi: 10.1101/gr.128124.111 . PubMed DOI PMC

Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34(17):i884–90. doi: 10.1093/bioinformatics/bty560 . PubMed DOI PMC

Chen S. Ultrafast one-pass FASTQ data preprocessing, quality control, and deduplication using fastp. iMeta. 2023;2(2):e107. doi: 10.1002/imt2.107 . PubMed DOI PMC

Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv preprint. 2013;1303.3997. doi: 10.48550/arxiv.1303.3997 DOI

Zaccaron AZ, Stergiopoulos I. Characterization of the mitochondrial genomes of three powdery mildew pathogens reveals remarkable variation in size and nucleotide composition. Microb Genom. 2021;7(12):000720. doi: 10.1099/mgen.0.000720 PubMed DOI PMC

Krumsiek J, Arnold R, Rattei T. Gepard: a rapid and sensitive tool for creating dotplots on genome scale. Bioinformatics. 2007;23(8):1026–8. doi: 10.1093/bioinformatics/btm039 . PubMed DOI

Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V, Pollard MO, et al.. Twelve years of SAMtools and BCFtools. Gigascience. 2021;10(2):giab008. doi: 10.1093/gigascience/giab008 . PubMed DOI PMC

Van der Auwera G, O’Connor B. Genomics in the cloud: Using Docker, GATK, and WDL in Terra. 2020.

Team R. R: A language and environment for statistical computing. 2022.

Paradis E, Schliep K. ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics. 2019;35(3):526–8. doi: 10.1093/bioinformatics/bty633 . PubMed DOI

Jombart T. adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24(11):1403–5. doi: 10.1093/bioinformatics/btn129 . PubMed DOI

Jombart T, Ahmed I. adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics. 2011;27(21):3070–1. doi: 10.1093/bioinformatics/btr521 . PubMed DOI PMC

Wickham H. ggplot2. Use R! 2016. doi: 10.1007/978-3-319-24277-4 DOI

Chang CC, Chow CC, Tellier LC, Vattikuti S, Purcell SM, Lee JJ. Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience. 2015;4:7. doi: 10.1186/s13742-015-0047-8 . PubMed DOI PMC

Korunes KL, Samuk K. pixy: Unbiased estimation of nucleotide diversity and divergence in the presence of missing data. Mol Ecol Resour. 2021;21(4):1359–68. doi: 10.1111/1755-0998.13326 . PubMed DOI PMC

Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, et al.. The variant call format and VCFtools. Bioinformatics. 2011;27(15):2156–8. doi: 10.1093/bioinformatics/btr330 . PubMed DOI PMC

Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123(3):585–95. doi: 10.1093/genetics/123.3.585 . PubMed DOI PMC

Gaunt TR, Rodríguez S, Day IN. Cubic exact solutions for the estimation of pairwise haplotype frequencies: implications for linkage disequilibrium analyses and a web tool “CubeX”. BMC Bioinformatics. 2007;8:428. doi: 10.1186/1471-2105-8-428 . PubMed DOI PMC

Saha S, Moorthi S, Wu X, Wang J, Nadiga S, Tripp P, et al.. The NCEP climate forecast system version 2. J Clim. 2014;27(6):2185–208. doi: 10.1175/jcli-d-12-00823.1 DOI

Nychka D, Furrer R, Paige J, Sain S. fields: Tools for spatial data. 2021.

Karger DN, Conrad O, Böhner J, Kawohl T, Kreft H, Soria-Auza RW, et al.. Climatologies at high resolution for the earth’s land surface areas. Sci Data. 2017;4:170122. doi: 10.1038/sdata.2017.122 . PubMed DOI PMC

Karger D, Conrad O, Böhner J, Kawohl T, Kreft H, Soria-Auza R. Climatologies at high resolution for the earth’s land surface areas. EnviDat. 2021. doi: 10.16904/envidat.228.v2.1 PubMed DOI PMC

Brun P, Zimmermann NE, Hari C, Pellissier L, Karger DN. Global climate-related predictors at kilometer resolution for the past and future. Earth Syst Sci Data. 2022;14(12):5573–603. doi: 10.5194/essd-14-5573-2022 DOI

Brun P, Zimmermann N, Hari C, Pellissier L, Karger D. CHELSA-BIOCLIM: A novel set of global climate-related predictors at kilometre-resolution. EnviDat. 2022. doi: 10.16904/envidat.332 DOI

Hijmans R. raster: Geographic Data Analysis and Modeling. 2022.

HarrellJr FE. rms: Regression Modeling Strategies. 2024. Available: https://CRAN.R-project.org/package=rms

Hunter JD. Matplotlib: A 2D Graphics Environment. Comput Sci Eng. 2007;9(3):90–5. doi: 10.1109/mcse.2007.55 DOI

Oksanen J, Simpson G, Blanchet F, Kindt R, Legendre P, Minchin P. vegan: Community Ecology Package. 2024.

Chartrain L, Brown JKM. Molecular evolution and mechanisms of fungicide resistance in plant pathogenic fungi. Burleigh Dodds Ser Agri Sci. 2023:21–58. doi: 10.19103/as.2022.0116.02 DOI

Martin M, Patterson M, Garg S, O Fischer S, Pisanti N, Klau GW, et al.. WhatsHap: fast and accurate read-based phasing. 2016. doi: 10.1101/085050 DOI

Csardi G, Nepusz T. The igraph software package for complex network research. Inter J. 2006;Complex Systems(1695).

Csárdi G, Nepusz T, Traag V, Horvát S, Zanini F, Noom D. igraph: Network analysis and visualization in R. 2024. doi: 10.5281/zenodo.7682609 DOI

Paradis E. pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics. 2010;26(3):419–20. doi: 10.1093/bioinformatics/btp696 . PubMed DOI

Himmelbach A, Zierold U, Hensel G, Riechen J, Douchkov D, Schweizer P, et al.. A set of modular binary vectors for transformation of cereals. Plant Physiol. 2007;145(4):1192–200. doi: 10.1104/pp.107.111575 . PubMed DOI PMC

Kunz L, Poretti M, Praz CR, Müller MC, Wyler M, Keller B, et al.. High-copy transposons from a pathogen give rise to a conserved sRNA family with a novel host immunity target. Mol Plant Microbe Interact. 2024;37(7):545–51. doi: 10.1094/MPMI-10-23-0176-SC . PubMed DOI

Weigel D, Glazebrook J. Transformation of agrobacterium using the freeze-thaw method. CSH Protoc. 2006;2006(7):pdb.prot4666. doi: 10.1101/pdb.prot4666 PubMed DOI

Zadoks JC, Chang TT, Konzak CF. A decimal code for the growth stages of cereals. Weed Res. 1974;14(6):415–21. doi: 10.1111/j.1365-3180.1974.tb01084.x DOI

Mains E, Diktz S. Physiologic forms of barley mildew, Erysiphe graminis hordei. Phytopathology. 1930;20:229–39.

Singh SP, Hurni S, Ruinelli M, Brunner S, Sanchez-Martin J, Krukowski P, et al.. Evolutionary divergence of the rye Pm17 and Pm8 resistance genes reveals ancient diversity. Plant Mol Biol. 2018;98(3):249–60. doi: 10.1007/s11103-018-0780-3 . PubMed DOI