Population genomics and molecular epidemiology of wheat powdery mildew in Europe

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.

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Publication Details

Journal
PLoS Biology
Published
2025-05-02
DOI
https://doi.org/10.1371/journal.pbio.3003097
Citations
7
Primary Topic
Wheat and Barley Genetics and Pathology
Type
article
Field-Weighted Citation Impact
12.25

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article

Population genomics and molecular epidemiology of wheat powdery mildew in Europe

Salim Bourras, Lukas Kunz, Candy McCabe, O. Cotuna et al.
7 citations
PLoS Biology
Wheat and Barley Genetics and Pathology
12.25
article

Population genomics and molecular epidemiology of wheat powdery mildew in Europe

Salim Bourras, Lukas Kunz, Candy McCabe, O. Cotuna, Steven Kildea, Angelica Giancaspro, Victoria Widrig, Jeanine Ly, Stefanos Testempasis, Nikolaos Minadakis, Žilvinas Liatukas, Neil Schwartz, Urszula Piechota, Roi Ben‐David, Kevin Gauthier, Antonín Dreiseitl, Sylwia Okoń, Gilles Couleaud, Matteo Bozzoli, G. S. Karaoglanidis, Fabrizio Menardo, Mónika Cséplö, Fernando Martínez–Moreno, Marta S. Lopes, Veronica SARATEANU, Stefania Lucia Giove, Charlotte F. Nellist, Dolors Villegas, Ágata Gadaleta, Ebubekir Koç, Francesca Desiderio, Amelia Hubbard, Javier Sánchez‐Martín, Virgilio Balmas, Jigisha Jigisha, Paweł Czembor, Angela Feechan, Ignacio Solís Martel, Thomas Miedaner, Beyhan Akın, Coraline R. Praz, Fabian Freund, Philipp Schulz, Szilvia Bencze, Fabio Mascher, Jost Dörnte, Alain Handley-Cornillet, Daniele Seghetta, Agrita Švarta
article en
7 citations

Abstract

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.

PLoS BiologyVol. 23(5)
University College Dublin (IE), University of Hohenheim (DE), Latvia University of Life Sciences and Technologies (LV), Julius Kühn-Institut (DE), Teagasc - The Irish Agriculture and Food Development Authority (IE), National Institute of Agricultural Botany (GB), University of Leicester (GB), Universitat de Lleida (ES), Deutsche Bank (Germany) (DE), University of Life Sciences in Lublin (PL), University of Sassari (IT), Universidad de Salamanca (ES), University of Zurich (CH), Aristotle University of Thessaloniki (GR), Swedish University of Agricultural Sciences (SE), West University of Timişoara (RO), Heriot-Watt University (GB), Agricultural Research Organization (IL), Centro di Ricerca per la Patologia Vegetale (IT), Agricultural Research Institute Kromeriz (CZ), Arvalis - Institut du Végétal (FR), Agroscope (CH), Estación Experimental de Aula Dei (ES), École Nationale Supérieure Agronomique (DZ), HUN-REN Centre for Agricultural Research (HU), Lithuanian Research Centre for Agriculture and Forestry (LT), Plant Breeding and Acclimatization Institute - National Research Institute (PL), Centre for Plant Biotechnology and Genomics (ES), Agricultural Institute (HU), Agrotest Fyto (Czechia), University of Bari Aldo Moro (IT), Research Institute of Organic Agriculture (BE), Universidad de Sevilla (ES), Univesity of Life Science "King Mihai I" from Timisoara (RO), Universidad Politécnica de Madrid (ES), University of Bologna (IT)
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
Zero hunger
Openalex Percentile: Top 2%
Wheat and Barley Genetics and Pathology
12.25
DOIOpen Access PDFOpenAlex
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