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

The non-vascular plant Marchantia polymorpha has emerged as a valuable model for studying evolutionarily conserved microbial infection strategies and plant immune responses. However, only a handful of fungal pathogens of Marchantia have been described so far. Here we establish a new pathosystem using the root-infecting vascular wilt fungus Fusarium oxysporum. On angiosperms, this fungus exhibits exquisite adaptation to the plant vascular niche and host-specific pathogenicity, both of which are conferred by lineage-specific effectors secreted during growth in the xylem. We show that F. oxysporum isolates with different lifestyles - pathogenic or endophytic - are able to infect this non-vascular liverwort causing tissue maceration and plant cell killing. Similar to bacterial pathogens, F. oxysporum induces a PAMP-triggered immune response in M. polymorpha. Analysis of isogenic fungal mutants established that infection of Marchantia requires conserved fungal pathogenicity mechanisms such as mitogen activated protein kinases, transcriptional regulators and cell wall remodeling enzymes. Remarkably, lineage-specific virulence effectors are dispensable for infection, most likely due to the absence of xylem tissue in this non-vascular plant. The F. oxysporum - M. polymorpha system provides new insights into the mechanism and evolution of pathogenic and endophytic fungus-plant interactions. Significance statementRoot-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 infect non-vascular plants, which diverged from vascular plants over 450 million years ago. Here we show that two strains of the fungus Fusarium oxysporum with opposed lifestyles, causing either wilting and death or beneficial protection on tomato, produce similar disease symptoms on the non-vascular plant Marchantia polymorpha. We define a set of core fungal pathogenicity factors required on both vascular and non-vascular plants and show that host-specific effectors contributing to disease on tomato are dispensable on Marchantia. These findings suggest that systemic wilt disease evolved in fungal pathogens after the emergence of vascular land plants.