Antonio Di Pietro: Transposons drive environmental adaptation in a clonally evolving fungal pathogen

The genomes of many fungal pathogens are compartmentalized into core regions and accessory regions, which are enriched in transposable elements (TEs). TEs are widely regarded as drivers of adaptive evolution, but direct experimental evidence remains limited. We used an evolve and re-sequence approach to follow environmental adaptation in Fusarium oxysporum, a devastating fungal pathogen that attacks more than 150 crops and causes deadly infections in immunocompromised humans. Serial passaging of a clonal isolate through tomato plants or axenic media plates resulted in rapid adaptation and increased fitness under the selection condition. Plate-passaged populations displayed recurrent evolutionary trajectories of sequential loss-of-function mutations that lead to increased proliferation at the cost of reduced virulence. TE insertions accounted for more than 70% of the variants detected and localized preferentially to sites of histone H3 lysine 27 trimethylation, a hallmark of accessory regions. Our findings show that TEs act as the main drivers of adaptation in F. oxysporum and reveal fitness trade-offs between developmental programs stimulating proliferation versus invasion.