A fusarioid fungus forms mutualistic interactions with poplar trees that resemble ectomycorrhizal symbiosis

<i>Fusarium</i> species, recognised as global priority pathogens, frequently induce severe diseases in crops; however, certain species exhibit alternative symbiotic lifestyles and are either non-pathogenic or endophytic. In this study, we characterised the mutualistic relationship between the eFp isolate of <i>F.pseudograminearum</i> and five poplar species, resulting in formation root structures reminiscent of ectomycorrhizal (ECM) symbiosis. This functional symbiosis is evidenced by enhanced plant growth, reciprocal nutrient exchange, improved nitrogen and phosphorus uptake and upregulation of root sugar transporter gene expression (<i>PtSweet1</i>). Comparative and population genomics confirmed that eFp maintains a structurally similar genome, but exhibits significant divergence from ten conspecific pathogenic isolates. Notably, eFp enhanced the growth of diverse plant lineages (<i>Oryza</i>, <i>Arabidopsis</i>, <i>Pinus</i> and non-vascular liverworts), indicating a near-complete loss of virulence. Although this specialised symbiosis has only been established <i>in vitro</i>, it holds significant value in elucidating the evolutionary track from endophytic to mycorrhizal associations.