Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen

Abstract

ABSTRACTPowdery mildews are biotrophic pathogenic fungi infecting a number of economically important plants. The grass powdery mildew,Blumeria graminis,has become a model organism to study host specialization of obligate biotrophic fungal pathogens. We resolved the large-scale genomic architecture ofB. graminis forma specialis hordei (Bgh)to explore the potential influence of its genome organization on the co-evolutionary process with its host plant, barley(Hordeum vulgare).The near-chromosome level assemblies of theBghreference isolate DH14 and one of the most diversified isolates, RACE1, enabled a comparative analysis of these haploid genomes, which are highly enriched with transposable elements (TEs). We found largely retained genome synteny and gene repertoires, yet detected copy number variation (CNV) of secretion signal peptide-containing protein-coding genes (SPs) and locally disrupted synteny blocks. Genes coding for sequence-related SPs are often locally clustered, but neither theSPclusters nor TEs are enriched in specific genomic regions. Extended comparative analysis with different host-specificB. graminis formae specialesrevealed the existence of a core suite ofSPs,but also isolate-specificSPsets as well as congruence ofSPCNV and phylogenetic relationship. We further detected evidence for a recent, lineage-specific expansion of TEs in theBghgenome. The characteristics of theBghgenome (largely retained synteny, CNV ofSPgenes, recently proliferated TEs and a lack of compartmentalization) are consistent with a “one-speed” genome that differs in its architecture and (co-)evolutionary pattern from the “two-speed” genomes reported for several other filamentous phytopathogens.