Copper acquisition is essential for plant colonization and virulence in a root-infecting vascular wilt fungus

Phytopathogenic fungi provoke devastating agricultural losses and are difficult to control. How fungal pathogens adapt to the plant environment to cause disease and complete their life cycle on the host remains poorly understood. Here we show that efficient acquisition of copper, mediated by the transcriptional regulator Mac1, is crucial for plant colonization and virulence in Fusarium oxysporum, a soilborne ascomycete that causes vascular wilt on more than 150 different crops. RNA-seq and ChIP-seq establish a direct role of Mac1 in activation of copper deficiency response genes, many of which are induced during plant infection. Loss of Mac1 impairs growth of F. oxysporum under copper-limiting condition as well as vascular colonization and virulence on tomato plants. Importantly, Mac1-independent overexpression of a copper reductase and a copper transporter restores growth under copper limitation and virulence in the mac1 null mutant background. These findings establish a key role for copper acquisition in fungal pathogenicity on plants and reveal new ways to protect crops from phytopathogens.