Two distinct Fusarium graminearum populations colonized European wheat in the past two decades

Abstract

Fusarium graminearum is the main causal agent of Fusarium head blight (FHB) disease in wheat in Europe. To reveal population structure and to pinpoint genetic targets of selection we studied genomes of 96 strains of F. graminearum using population genomics. Bayesian and phylogenomic analyses indicated that the F. graminearum emergence in Europe could be linked to two independently evolving populations termed here as East European (EE) and West European (WE) population. The EE strains are primarily prevalent in Eastern Europe, but to a lesser extent also in western and southern areas. In contrast, the WE population appears to be endemic to Western Europe. Both populations evolved in response to population-specific selection forces, resulting in distinct localized adaptations that allowed them to migrate into their environmental niche. The detection of positive selection in genes with protein/zinc ion binding domains, transcription factors and in genes encoding proteins involved in transmembrane transport highlights their important role in driving evolutionary novelty that allow F. graminearum to increase adaptation to the host and/or environment. F. graminearum also maintained distinct sets of accessory genes showing population-specific conservation. Among them, genes involved in host invasion and virulence such as those encoding proteins with high homology to tannase/feruloyl esterase and genes encoding proteins with functions related to oxidation-reduction were mostly found in the WE population. Our findings shed light on genetic features related to microevolutionary divergence of F. graminearum and reveal relevant genes for further functional research aiming at better control of this pathogen.