Long-distance gene flow and recombination shape the evolutionary history of a maize pathogen

The evolutionary history of crop pathogens is shaped by a complex interaction of natural and anthropogenic factors. The fungus <i>Colletotrichumgraminicola</i> causes maize anthracnose which results in significant yield losses worldwide. We conducted a comprehensive investigation into the evolutionary genomics of <i>C.graminicola</i> using a collection of 212 isolates from 17 countries across five continents. Genomic analyses supported the existence of three geographically isolated genetic lineages, with a significant pattern of isolation by distance. We identified two distinct gene flow patterns, driven by short- and long-distance dispersal, likely resulting from the natural spread of the pathogen and the exchange of contaminated seeds. We present evidence of genetic introgression between lineages, suggesting a long history of recombination. We identified significant recombination events coalescing at distinct points in time, with the North American lineage displaying evidence of the most ancient recombination. Demographic modelling has indicated that North America is an intermediate between Brazil, Europe and an ancestral, unsampled source population, which is hypothesised to be Mesoamerican. Our analyses revealed that the global genomic structure of <i>C.graminicola</i> is shaped by geographic differentiation driven by long-distance migration and a long history of recombination and introgression. We show historical relationships amongst these lineages, identifying a potential route for fungal spread, with the North American population emerging ancestrally, followed sequentially by the Brazilian and European populations. Our research indicates that the European lineage is more virulent, which has implications for the potential emergence of new outbreaks of maize anthracnose in Europe.

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Publication Details

Journal
IMA Fungus
Published
2025-02-21
DOI
https://doi.org/10.3897/imafungus.16.138888
Citations
1
Primary Topic
Plant Virus Research Studies
Type
article
Field-Weighted Citation Impact
1.75

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article

Long-distance gene flow and recombination shape the evolutionary history of a maize pathogen

Ivica Buhiniček, Guilherme Kenichi Hosaka, Pedro Revilla, Serenella A. Sukno et al.
1 citations
IMA Fungus
Plant Virus Research Studies
1.75
article

Long-distance gene flow and recombination shape the evolutionary history of a maize pathogen

Ivica Buhiniček, Guilherme Kenichi Hosaka, Pedro Revilla, Serenella A. Sukno, Pablo García-Rodríguez, Sioly Becerra, Jürg Hiltbrunner, Rogelio Santiago, Stéphane De Mita, José Luis Vicente Villardón, W. Bettiol, Cock van Oosterhout, Andrés G. Jacquat, Flávia Rogério, Francisco Borja Cuevas-Fernández, José S. Dambolena, Michael R. Thon, Silvia Gutiérrez-Sánchez, Sofia B. Ulla
article en
1 citations

Abstract

The evolutionary history of crop pathogens is shaped by a complex interaction of natural and anthropogenic factors. The fungus <i>Colletotrichumgraminicola</i> causes maize anthracnose which results in significant yield losses worldwide. We conducted a comprehensive investigation into the evolutionary genomics of <i>C.graminicola</i> using a collection of 212 isolates from 17 countries across five continents. Genomic analyses supported the existence of three geographically isolated genetic lineages, with a significant pattern of isolation by distance. We identified two distinct gene flow patterns, driven by short- and long-distance dispersal, likely resulting from the natural spread of the pathogen and the exchange of contaminated seeds. We present evidence of genetic introgression between lineages, suggesting a long history of recombination. We identified significant recombination events coalescing at distinct points in time, with the North American lineage displaying evidence of the most ancient recombination. Demographic modelling has indicated that North America is an intermediate between Brazil, Europe and an ancestral, unsampled source population, which is hypothesised to be Mesoamerican. Our analyses revealed that the global genomic structure of <i>C.graminicola</i> is shaped by geographic differentiation driven by long-distance migration and a long history of recombination and introgression. We show historical relationships amongst these lineages, identifying a potential route for fungal spread, with the North American population emerging ancestrally, followed sequentially by the Brazilian and European populations. Our research indicates that the European lineage is more virulent, which has implications for the potential emergence of new outbreaks of maize anthracnose in Europe.

IMA FungusVol. 16
University of East Anglia (GB), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (FR), Universidad Nacional de Córdoba (AR), Universidade de São Paulo (BR), Universidad de Salamanca (ES), Université de Montpellier (FR), Brazilian Agricultural Research Corporation (BR), Institut Agro Montpellier (FR), University of Florida (US), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), Methodist University of Piracicaba (BR), Misión Biológica de Galicia (ES), Agroscope (CH)
Universidad de Málaga, Institut Français de Bioinformatique, European Commission, Agence Nationale de la Recherche, Earth and Life Systems Alliance, Junta de Castilla y León, Smithsonian Conservation Biology Institute, European Regional Development Fund, Agencia Estatal de Investigación
Openalex Percentile: Top 17%
Plant Virus Research Studies
1.75
DOIOpen Access PDFOpenAlex
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