Host adaptation in the cross-kingdom pathogen Fusarium oxysporum

Fungal pathogens pose a severe threat to human health and food security. These organisms often show exquisite host adaptation, but also undergo rapid evolution leading to shifts or expansions in the host range. The genetic mechanisms of pathogen-host adaptation remain poorly understood. In the soil-inhabiting vascular wilt fungus Fusarium oxysporum, individual isolates tend to exhibit high specificity towards a given plant host, while the species complex collectively attacks more than a hundred different crops. In addition, F. oxysporum is also an emerging human pathogen that provokes lethal systemic infections in immunocompromised individuals. Remarkably, a single field isolate of this fungus can kill tomato plants, immunodepressed mice and insects. By following a combination of reverse genetics and experimental evolution approaches, we found that F. oxysporum uses multiple strategies to adapt to different host environments. These include the recruitment of conserved cell signaling pathways or hijacking of host regulatory mechanisms. Fungal populations obtained after serial passages through different environments displayed significant alterations in growth, development and virulence phenotypes compared to the original clone. Re-sequencing of evolved populations revealed changes both at the nucleotide and chromosome level, many of which were fixed in the population. Our results suggest that genome plasticity acts as a major evolutionary driver in F. oxysporum, and that host adaptation involves trade-offs between developmental programs favouring infection versus proliferation.