Abstract
Genome analyses have revealed a profound role of hybridization and introgression in the evolution of many eukaryote lineages, including fungi. The impact of recurrent introgression on fungal evolution however remains elusive. Here, we analyzed signatures of introgression along the genome of the fungal wheat pathogen Zymoseptoria tritici. We applied a comparative population genomics approach, including genome data from five Zymoseptoria species, to characterize the distribution and composition of introgressed regions representing segments with an exceptional haplotype pattern. These regions are found throughout the genome, comprising 5% of the total genome and overlapping with > 1,000 predicted genes. We performed window-based phylogenetic analyses along the genome to distinguish regions which have a monophyletic or nonmonophyletic origin with Z. tritici sequences. A majority of nonmonophyletic windows overlap with the highly variable regions suggesting that these originate from introgression. We verified that incongruent gene genealogies do not result from incomplete lineage sorting by comparing the observed and expected length distribution of haplotype blocks resulting from incomplete lineage sorting. Although protein-coding genes are not enriched in these regions, we identify 18 that encode putative virulence determinants. Moreover, we find an enrichment of transposable elements in these regions implying that hybridization may contribute to the horizontal spread of transposable elements. We detected a similar pattern in the closely related species Zymoseptoria ardabiliae, suggesting that hybridization is widespread among these closely related grass pathogens. Overall, our results demonstrate a significant impact of recurrent hybridization on overall genome evolution of this important wheat pathogen.
Highlights
Previous studies of fungal pathogen genomes have revealed exceptionally high levels of genomic variability (Möller & Stukenbrock 2017)
We included one genome each of Z. ardabiliae, Z. brevis, and Z. pseudotritici sequenced with PacBio technology and one genome of Z. passerinii sequenced with Illumina technology (Stukenbrock et al, 2011)
We defined a threshold to distinguish windows with more than 200 segregating sites within 1kb-windows as highly variable windows, and we joined consecutive windows in this category to have a map of highly variable regions (HVRs) along the Z. tritici genome
Summary
Previous studies of fungal pathogen genomes have revealed exceptionally high levels of genomic variability (Möller & Stukenbrock 2017). Some of this variation is considered adaptive, allowing pathogens to cope with variation in host immune genes and overcome immune responses leading to infection in plant host tissues. Analyses of genome data have revealed new insights on howhybridization can provide a mechanism for the emergence of new plant pathogens and novel host specificities within few years (Stukenbrock et al 2012; Menardo et al 2016; Depotter et al 2018). Hybridization gave rise to a new mildew pathogen on the crop species triticale, a hybrid cereal that was introduced in the 1960s (Menardo et al 2016). Introgressive hybridization was shown to contribute to the genome evolution of other important fungal crop pathogens including Verticillium longisporum causing stem striping disease on oilseed rape andthe apple scab pathogen Venturia inaequalis (Depotter et al 2017; Leroy et al 2016b)
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