Rogério Flávia, Van Oosterhout Cock, De Mita Stéphane, Cuevas-Fernández Francisco Borja, García-Rodríguez Pablo, Becerra Sioly, Gutiérrez-Sánchez Silvia, Jacquat Andrés G, Bettiol Wagner, Hosaka Guilherme Kenichi, Ulla Sofia B, Hiltbrunner Jürg, Santiago Rogelio, Revilla Pedro, Dambolena José S, Vicente-Villardón José L, Buhiniček Ivica, Sukno Serenella A, Thon Michael R
Department of Microbiology and Genetics, Institute for Agribiotechnology Research (CIALE), University of Salamanca, Villamayor, Salamanca, Spain.
Present Address: Department of Plant Pathology, University of Florida, Gainesville, Florida 32611, USA.
IMA Fungus. 2025 Feb 21;16:e138888. doi: 10.3897/imafungus.16.138888. eCollection 2025.
The evolutionary history of crop pathogens is shaped by a complex interaction of natural and anthropogenic factors. The fungus causes maize anthracnose which results in significant yield losses worldwide. We conducted a comprehensive investigation into the evolutionary genomics of 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 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.
作物病原体的进化史受到自然和人为因素复杂相互作用的影响。这种真菌会引发玉米炭疽病，在全球范围内导致重大产量损失。我们利用来自五大洲17个国家的212个分离株，对其进化基因组学进行了全面调查。基因组分析支持存在三个地理隔离的遗传谱系，呈现出显著的距离隔离模式。我们识别出由短距离和长距离扩散驱动的两种不同的基因流动模式，这可能是病原体自然传播和受污染种子交换的结果。我们提供了谱系间基因渐渗的证据，表明存在长期的重组历史。我们识别出在不同时间点合并的显著重组事件，北美谱系显示出最古老重组的证据。种群动态建模表明，北美是巴西、欧洲和一个未采样的祖先种群之间的中间地带，推测该祖先种群位于中美洲。我们的分析表明，该真菌的全球基因组结构是由长距离迁移驱动的地理分化以及长期的重组和基因渐渗所塑造的。我们展示了这些谱系之间的历史关系，确定了真菌传播的潜在途径，北美种群在祖先时期出现，随后依次是巴西和欧洲种群。我们的研究表明欧洲谱系毒性更强，这对欧洲玉米炭疽病新疫情的潜在出现具有影响。
