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.

Fig 1. Population structure analysis of F. graminearum populations.

(a) Principal component analysis (PCA) of a set of F. graminearum strains detecting three distinct populations: A1, East European (EE) and West European (WE). Legend: A1 includes seven strains of diverse geographical origin. (b) Evolutionary history and genetic structure of European populations of F. graminearum. Legend: A maximum-likelihood (ML) phylogeny inferred from SNPs identified by reference-based mapping of whole genome sequences to the reference PH-1 strain (accession number GCF_000240135.3). Three different colors indicate clustering assignment of each isolate in the three populations inferred from Bayesian analyses: A1 = yellow, East European (EE) = green and West European (WE) = purple. Strains marked with red font indicate admixed strains. Six strains from FGSC were chosen as outgroup: F. boothii (CBS 110251 and CBS 119170), and F. louisianense (CBS 127524 and CBS 127525) and F. gerlachii (CBS 119175 and CBS 119176). The tree was rooted with F. boothii and drawn to scale, with branch lengths measured in the number of substitutions per site. (c) A phylogenetic network constructed from a set of F. graminearum strains by reference-based mapping to the reference PH-1 strain. Legend: Strains are represented by terminal nodes, and relationships are depicted as branches with parallel edges indicating recombination and/or gene transfer. Strains marked with red font indicate admixed strains.

Fig 2. Linkage disequilibrium (LD) decay between pairs of SNPs, measured as R2, with distance on the same scaffold.

Fig 3. Genetic variation of TRI genes leading to formation of NIV, 3-AcDON, 15-AcDON and NX-2 genotypes.

Fig 4. Distribution of outliers with signatures of selection.

Legend: Sliding-window values of interpopulation differentiation (Panel B, Tajima’s D (estimated as a relative measure of inter-population divergence for pooled populations), D_xy (nucleotide divergence based on the absolute number of differences between two populations), and F_ST (per haplotype, adjusted for unequal population sizes using weighted averages) were calculated in 10 kb windows to identify outliers in both East European (EE) and West European (WE) populations. The nine outliers (o1-o9) showed significant (P-value < 0.05) divergence between populations based on pairwise (interpopulation) values of Tajima’s D, D_xy, and F_ST, coupled with significantly reduced diversity (π) within the populations. Significance was assessed by comparing observed sliding-window values of each metric against a null genome-wide distribution derived through random permutation.