Genome plasticity mediated by transposable elements drives the evolution of virulence in the vascular wilt pathogen Verticillium dahliae

Verticillium dahliae is a soil-borne pathogen that aggressively colonizes hundreds of host plants, including high value crops such as tomato and potato, leading to the formation of vascular wilt disease. Resistance in the host population exert selective pressure on the pathogen forcing the rapid evolution of adaptive traits to successfully participate in the arms race with the host. By comparative genomics of the V. dahliae population, we recently revealed genomic rearrangements that facilitate the gain and loss of genetic material and establish highly dynamic lineage-specific (LS) regions. LS regions are enriched for transposable elements (TEs) and in planta induced effector genes encoding secreted protein that significantly contribute to aggressiveness towards the host, and thus have been hypothesized to contribute to the genome plasticity required for adaptive genome evolution. However, the factors that drive genome plasticity in V. dahliae remain enigmatic. Using long-read sequencing technologies, we re-sequenced two V. dahliae strains and analyzed the previously identified genomic rearrangements in unprecedented detail, revealing multiple genomic breakpoints down to the nucleotide level. Genomic breakpoints are flanked by multiple TEs, suggesting that these elements play essential roles in their formation. Comparative analyses of V. dahliae with the recently sequenced non-pathogenic Verticillium tricorpus revealed a highly expanded TE repertoire in pathogenic V. dahliae, where in planta induced effector candidates, but also other genes encoding secreted proteins, are frequently flanked by TEs. Additionally, whole-genome bisulfite sequencing of V. dahliae identified DNA methylation predominantly targeting TEs. In fungi, inactivation of TEs by DNA methylation is common, and we hypothesize that it could also influence the expression of nested effector candidates, thereby providing yet another route how TEs can affect the interaction between the pathogen and its host. In summary, we highlight the profound role of TEs on the evolution of virulence in the vascular wilt pathogen V. dahliae.