The genomic architecture of the grape powdery mildew pathogen Erysiphe necator and its impact on the pathogen’s biology and virulence

Erysiphe necator causes grape powdery mildew, globally the most important fungal disease on grapevines. The current reference genome assembly of the pathogen is highly fragmented due to its repetitive DNA content, which prevents a detailed analysis of its genomic architecture. Here, we present an 81.1 Mb genome assembly for E. necator that is 98% complete and consists of 34 scaffolds, 11 of which represent complete chromosomes. Analysis of the chromosomes’ content showed that they all contain large centromeric-like regions that account for 15.8% of the genome. Repeats and transposable elements (TEs) represent 62.7% of their content and, while they are almost evenly interspersed outside centromeric and telomeric regions, they massively overlap with regions of annotated genes, indicating that they could have a significant impact on their evolution. Indeed, abundant gene duplicates were observed, particularly in genes encoding candidate secreted effector proteins (CSEPs) that could have been spawned by TE activity. Copies of duplicated CSEP-encoding genes were further found to be frequently clustered in the genome, suggesting recurrent events of local gene duplications and adaptive variation. Finally, in accordance with the obligate biotrophic nature of E. necator, abundant losses in genes needed to synthesize metabolites that can be obtained directly through the host environment were also observed. These and other genomic architectural features of E. necator will be discussed.