A recent shift in centromere size and DNA content in Podospora pseudocomata co-occurs with the loss of a fungal genome defense system

The centromere of the eukaryotic chromosome is necessary for the accurate segregation during cell division. Yet, centromeric DNA is highly variable and rapidly evolving. In fungi, centromeres range from point- to regional centromeres, some of which are hundreds of thousands of base pairs long and filled with transposable elements. As fungi have evolved several specialized defense mechanisms against transposable elements, these regional centromeres are intriguing sites for investigating the connection between genome defense and centromere evolution. Here, we investigated the structure of the centromeres of seven species of the Podospora anserina species complex, which is made up of closely related filamentous ascomycetes that diverged less than 1 MYA. We discovered that one species in the complex, P. pseudocomata, lacks the genomic signature of the specialized genome defense mechanism called Repeat Induced Point mutations (RIP). We identified the centromeric regions in P. anserina and P. pseudocomata using chromatin immunoprecipitation targeting the centromere-specific histone variant cenH3, and using comparative genomics we inferred the size of centromeric regions in the other species. We found that while the centromere structure in the complex is generally well conserved, the centromeric regions of P. pseudocomata has gone through a rapid change. Specifically, the size of the centromeres in P. pseudocomata are 35-46 kb, which is significantly smaller than those of the other species (44-90 kb), and the DNA-transposon discoglosse is the most abundant TE family instead of the typical LTR-retrotransposon crapaud. Taken together, our data strongly indicates a link between genome defense and centromere evolution in fungi.