Genome plasticity impacts adaptive genome evolution in the vascular wilt pathogen Verticillium

Genome plasticity enables organisms to adapt to environmental changes and to occupy novel niches. This is established by mechanisms ranging from single-nucleotide polymorphisms to large-scale chromosomal variations, all of which contribute to differences in chromosomal size, organization and gene content. While these mechanisms operate in all organisms, they are particularly relevant for plant pathogens that engage in a co-evolutionary arms race with their hosts. Plant pathogens secrete so-called effectors that contribute to host colonization and counteract host immunity. Effector genes often cluster in highly plastic, transposon-rich genomic regions. However, mechanistic understanding of the evolution of these plastic genomic regions remains scarce. We study these molecular mechanisms in the fungal genus Verticillium that contains economically and ecologically important plant pathogens, among which Verticillium dahliae is the most notorious pathogen that causes vascular wilt disease on >200 plant species. Using long-read sequencing technology, we completely assembled two V. dahliae strains. By comparative genomics, we established that transposable elements play important roles in shaping the genome of V. dahliae. Plastic genomic regions in V. dahliae that contain all known effectors evolve by extensive genomic rearrangements that are mediated by erroneous double-strand breaks, often over transposons. Extensive genomic rearrangements are not only restricted to V. dahliae, but also occur in related Verticillium species. Furthermore, recent segmental duplications are enhanced in the plastic regions. These regions, in contrast to the core genome, are also enriched in active transposons that further contribute to local plasticity. In fungi, transposons are located in tightly condensed chromatin, so called heterochromatin, that is supposed to suppress transposon activity and repress structural variations. In contrast, many fungal pathogens have highly plastic transposon-rich regions. Therefore, research into chromatin opens new avenues to link genome organization, genome plasticity and adaptive genome evolution in fungal pathogens.