Combining pangenomics and population genetics finds chromosomal re-arrangements, accessory-like chromosome segments, copy number variations and transposon polymorphisms in wheat and rye powdery mildew

Grass powdery mildews (Blumeria spp.) include economically important fungal crop pathogens with complex and highly repetitive genomes. To investigate the diversity and genome evolution in Blumeria graminis, we combined population genetic and pangenomic analyses using a worldwide sample of 399 wheat powdery mildew isolates. Additionally, we produced high-quality genome assemblies for seven isolates from wheat and one from rye powdery mildew. Using these, we compiled the first grass powdery mildew pangenome comprising 11 Blumeria graminis isolates. We found multiple chromosomal rearrangements between the isolates that grow on wheat, rye and/or triticale hosts. Interestingly, chr-11 showed some characteristics of accessory chromosomes such as presence/absence of large chromosomal segments and higher sequence diversity. Additionally, we identified nearly 67,000 cases of copy number variations (CNVs), which were highly enriched within effector gene families. Furthermore, we found evidence for recent and high transposable element (TE) activity, such as high numbers of TE insertion polymorphisms. Analyses of TE families showed enrichment 1 kb to 2 kb up- and downstream of effector genes, and we also found high levels of TE insertion polymorphisms between populations. Our results demonstrate that chromosomal variations, gene family expansions and contractions, and TE activity are important sources of genome diversification and diversity in grass powdery mildews. Our findings indicate that a combination of pangenomic and population genetics analyses is needed to understand drivers of evolution in plant pathogenic fungi in a comprehensive way. Author SummaryFungi are a diverse group of organisms, with some of them (e.g. powdery mildews) having at times a devastating impact on important crops like wheat. Studying the genomes of these grass powdery mildew fungi can improve our understanding the pathogens patterns of genome evolution and virulence in order to find more efficient ways to protect crops. Using high quality genomes of a worldwide dataset of wheat and rye powdery mildews, we found multiple re-arrangements in chromosomes, as well as presence and absence of large chromosomal segments in different mildew strains. Along with some genes, important for making these pathogens infectious on various crop lines, some genomic regions may be deleted or duplicated, potentially affecting how the fungus survives and spreads. Additionally, we found that transposable elements are highly active in powdery mildews and that they are enriched near so-called effector genes, which are associated with fungal virulence. Our study shows how powdery mildew genomes have diversified during recent evolution, which has implications for future breeding of crops toward better resistance to fungal diseases.