Marchantia polymorpha model reveals conserved infection mechanisms in the vascular wilt fungal pathogen Fusarium oxysporum.

Root-infecting vascular fungi cause wilt diseases and provoke devastating losses in hundreds of crops. It is currently unknown how these pathogens evolved and whether they can also infect non-vascular plants, which diverged from vascular plants over 450 million years ago. We established a pathosystem between the non-vascular plant Marchantia polymorpha (Mp) and the root-infecting vascular wilt fungus Fusarium oxysporum (Fo). On angiosperms, Fo exhibits exquisite adaptation to the plant xylem niche as well as host-specific pathogenicity, both of which are conferred by effectors encoded on lineage-specific (LS) chromosomes. Fo isolates displaying contrasting lifestyles on angiosperms - pathogenic versus endophytic - are able to infect Mp and cause tissue maceration and host cell killing. Using isogenic fungal mutants we define a set of conserved fungal pathogenicity factors, including mitogen activated protein kinases, transcriptional regulators and cell wall remodeling enzymes, that are required for infection of both vascular and non-vascular plants. Remarkably, two host-specific effectors and a morphogenetic regulator, which contribute to vascular colonization and virulence on tomato plants are dispensable on Mp. Collectively, these findings suggest that vascular wilt fungi employ conserved infection strategies on non-vascular and vascular plant lineages but also have specific mechanisms to access the vascular niche of angiosperms.