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...

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Autores: Jigisha, Jigisha, Ly, Jeanine, Minadakis, Nikolaos, Freund, Fabian, Kunz, Lukas, Piechota, Urszula, Akin, Beyhan, Balmas, Virgilio, Ben-David, Roi, Bourras, Salim, Bozzoli, Matteo, Cotuna, Otilia, Couleaud, Gilles, Cséplő, Mónika, Czembor, Paweł, Desiderio, Francesca, Dörnte, Jost, Dreiseitl, Antonín, Feechan, Angela, Gadaleta, Agata, Gauthier, Kevin, Giancaspro, Angelica, Giove, Stefania L., Handley-Cornillet, Alain, Hubbard, Amelia, Karaoglanidis, George, Kildea, Steven, Koc, Emrah, Liatukas, Žilvinas, da Silva Lopes, Marta, Mascher, Fabio, McCabe, Cathal, Miedaner, Thomas, Martínez-Moreno, Fernando, Nellist, Charlotte F., Okoń, Sylwia, Praz, Coraline, Sánchez-Martín, Javier, Sărăţeanu, Veronica, Schulz, Philipp, Schwartz, Nathalie, Seghetta, Daniele, Solís Martel, Ignacio, Švarta, Agrita, Testempasis, Stefanos, Villegas, Dolors, Widrig, Victoria, Menardo, Fabrizio
Tipo de recurso: artículo
Fecha de publicación:2025
País:España
Institución:Institut de Recerca i Tecnologia Agroalimentàries (IRTA)
Repositorio:IRTA Pubpro. Open Digital Archive
OAI Identifier:oai:repositori.irta.cat:20.500.12327/4559
Acceso en línea:http://hdl.handle.net/20.500.12327/4559
https://doi.org/10.1371/journal.pbio.3003097
Access Level:acceso abierto
Palabra clave:632
633
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spelling Population genomics and molecular epidemiology of wheat powdery mildew in EuropeJigisha, JigishaLy, JeanineMinadakis, NikolaosFreund, FabianKunz, LukasPiechota, UrszulaAkin, BeyhanBalmas, VirgilioBen-David, RoiBourras, SalimBozzoli, MatteoCotuna, OtiliaCouleaud, GillesCséplő, MónikaCzembor, PawełDesiderio, FrancescaDörnte, JostDreiseitl, AntonínFeechan, AngelaGadaleta, AgataGauthier, KevinGiancaspro, AngelicaGiove, Stefania L.Handley-Cornillet, AlainHubbard, AmeliaKaraoglanidis, GeorgeKildea, StevenKoc, EmrahLiatukas, Žilvinasda Silva Lopes, MartaMascher, FabioMcCabe, CathalMiedaner, ThomasMartínez-Moreno, FernandoNellist, Charlotte F.Okoń, SylwiaPraz, CoralineSánchez-Martín, JavierSărăţeanu, VeronicaSchulz, PhilippSchwartz, NathalieSeghetta, DanieleSolís Martel, IgnacioŠvarta, AgritaTestempasis, StefanosVillegas, DolorsWidrig, VictoriaMenardo, Fabrizio632633Agricultural 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.info:eu-repo/semantics/publishedVersionPublic Library of ScienceProducció VegetalCultius Extensius SosteniblesBencze, Szilvia202520252025info:eu-repo/semantics/article32application/pdfhttp://hdl.handle.net/20.500.12327/4559https://doi.org/10.1371/journal.pbio.3003097reponame:IRTA Pubpro. Open Digital Archiveinstname:Institut de Recerca i Tecnologia Agroalimentàries (IRTA)InglésPlos BiologyAttribution 4.0 Internationalhttp://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.irta.cat:20.500.12327/45592026-06-16T08:51:17Z
dc.title.none.fl_str_mv Population genomics and molecular epidemiology of wheat powdery mildew in Europe
title Population genomics and molecular epidemiology of wheat powdery mildew in Europe
spellingShingle Population genomics and molecular epidemiology of wheat powdery mildew in Europe
Jigisha, Jigisha
632
633
title_short Population genomics and molecular epidemiology of wheat powdery mildew in Europe
title_full Population genomics and molecular epidemiology of wheat powdery mildew in Europe
title_fullStr Population genomics and molecular epidemiology of wheat powdery mildew in Europe
title_full_unstemmed Population genomics and molecular epidemiology of wheat powdery mildew in Europe
title_sort Population genomics and molecular epidemiology of wheat powdery mildew in Europe
dc.creator.none.fl_str_mv Jigisha, Jigisha
Ly, Jeanine
Minadakis, Nikolaos
Freund, Fabian
Kunz, Lukas
Piechota, Urszula
Akin, Beyhan
Balmas, Virgilio
Ben-David, Roi
Bourras, Salim
Bozzoli, Matteo
Cotuna, Otilia
Couleaud, Gilles
Cséplő, Mónika
Czembor, Paweł
Desiderio, Francesca
Dörnte, Jost
Dreiseitl, Antonín
Feechan, Angela
Gadaleta, Agata
Gauthier, Kevin
Giancaspro, Angelica
Giove, Stefania L.
Handley-Cornillet, Alain
Hubbard, Amelia
Karaoglanidis, George
Kildea, Steven
Koc, Emrah
Liatukas, Žilvinas
da Silva Lopes, Marta
Mascher, Fabio
McCabe, Cathal
Miedaner, Thomas
Martínez-Moreno, Fernando
Nellist, Charlotte F.
Okoń, Sylwia
Praz, Coraline
Sánchez-Martín, Javier
Sărăţeanu, Veronica
Schulz, Philipp
Schwartz, Nathalie
Seghetta, Daniele
Solís Martel, Ignacio
Švarta, Agrita
Testempasis, Stefanos
Villegas, Dolors
Widrig, Victoria
Menardo, Fabrizio
author Jigisha, Jigisha
author_facet Jigisha, Jigisha
Ly, Jeanine
Minadakis, Nikolaos
Freund, Fabian
Kunz, Lukas
Piechota, Urszula
Akin, Beyhan
Balmas, Virgilio
Ben-David, Roi
Bourras, Salim
Bozzoli, Matteo
Cotuna, Otilia
Couleaud, Gilles
Cséplő, Mónika
Czembor, Paweł
Desiderio, Francesca
Dörnte, Jost
Dreiseitl, Antonín
Feechan, Angela
Gadaleta, Agata
Gauthier, Kevin
Giancaspro, Angelica
Giove, Stefania L.
Handley-Cornillet, Alain
Hubbard, Amelia
Karaoglanidis, George
Kildea, Steven
Koc, Emrah
Liatukas, Žilvinas
da Silva Lopes, Marta
Mascher, Fabio
McCabe, Cathal
Miedaner, Thomas
Martínez-Moreno, Fernando
Nellist, Charlotte F.
Okoń, Sylwia
Praz, Coraline
Sánchez-Martín, Javier
Sărăţeanu, Veronica
Schulz, Philipp
Schwartz, Nathalie
Seghetta, Daniele
Solís Martel, Ignacio
Švarta, Agrita
Testempasis, Stefanos
Villegas, Dolors
Widrig, Victoria
Menardo, Fabrizio
author_role author
author2 Ly, Jeanine
Minadakis, Nikolaos
Freund, Fabian
Kunz, Lukas
Piechota, Urszula
Akin, Beyhan
Balmas, Virgilio
Ben-David, Roi
Bourras, Salim
Bozzoli, Matteo
Cotuna, Otilia
Couleaud, Gilles
Cséplő, Mónika
Czembor, Paweł
Desiderio, Francesca
Dörnte, Jost
Dreiseitl, Antonín
Feechan, Angela
Gadaleta, Agata
Gauthier, Kevin
Giancaspro, Angelica
Giove, Stefania L.
Handley-Cornillet, Alain
Hubbard, Amelia
Karaoglanidis, George
Kildea, Steven
Koc, Emrah
Liatukas, Žilvinas
da Silva Lopes, Marta
Mascher, Fabio
McCabe, Cathal
Miedaner, Thomas
Martínez-Moreno, Fernando
Nellist, Charlotte F.
Okoń, Sylwia
Praz, Coraline
Sánchez-Martín, Javier
Sărăţeanu, Veronica
Schulz, Philipp
Schwartz, Nathalie
Seghetta, Daniele
Solís Martel, Ignacio
Švarta, Agrita
Testempasis, Stefanos
Villegas, Dolors
Widrig, Victoria
Menardo, Fabrizio
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Producció Vegetal
Cultius Extensius Sostenibles
Bencze, Szilvia
dc.subject.none.fl_str_mv 632
633
topic 632
633
description 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.
publishDate 2025
dc.date.none.fl_str_mv 2025
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv http://hdl.handle.net/20.500.12327/4559
https://doi.org/10.1371/journal.pbio.3003097
url http://hdl.handle.net/20.500.12327/4559
https://doi.org/10.1371/journal.pbio.3003097
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Plos Biology
dc.rights.none.fl_str_mv Attribution 4.0 International
http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv Attribution 4.0 International
http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 32
application/pdf
dc.publisher.none.fl_str_mv Public Library of Science
publisher.none.fl_str_mv Public Library of Science
dc.source.none.fl_str_mv reponame:IRTA Pubpro. Open Digital Archive
instname:Institut de Recerca i Tecnologia Agroalimentàries (IRTA)
instname_str Institut de Recerca i Tecnologia Agroalimentàries (IRTA)
reponame_str IRTA Pubpro. Open Digital Archive
collection IRTA Pubpro. Open Digital Archive
repository.name.fl_str_mv
repository.mail.fl_str_mv
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