Evolution of virulence in the vascular wilt pathogen Verticillium dahliae

Fungi cause severe crop losses and threaten food security worldwide. The soil-borne fungal pathogen Verticillium dahliae causes vascular wilt disease on hundreds of plant species, and disease control is challenging because resistance in plants is relatively rare. Moreover, V. dahliae has a flexible genome allowing it to escape host immunity and maintain aggressiveness. So far, knowledge on mechanisms governing this genomic flexibility remains limited. Through comparative population genomics we have started to unravel mechanisms to establish the genomic diversity that is essential for adaptive genome co-evolution during the continued arms race with host plants. To this end, two V. dahliae genomes were assembled from telomere-to-telomere using long-read sequencing technology and optical mapping, and compared these to the genomes of other Verticillium spp., revealing a pre-speciation genome duplication event. Comparative genomics using the two finished V. dahliae genomes furthermore revealed recent segmental duplications that established lineage-specific regions. Interestingly, these regions are enriched for in planta-expressed effector genes encoding secreted proteins that enable host colonization, and thus contribute to the evolution of virulence. Our evidence suggests that error-prone homology-dependent DNA repair has caused genomic rearrangements, leading to extensive structural variations. Re-sequencing of additional strains showed that independent losses of genetic material favored the escape of host recognition and, likely, host specificity. We propose that evolution of V. dahliae is linked to segmental genome duplications mediated by improperly repaired DNA breaks.