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Summary  During infection, soilborne fungal pathogens face limiting conditions of different metal ions, including zinc. The role of zinc homeostasis in fungal pathogenicity on plants remains poorly understood. Here it is shown that the transcription factor ZafA, orthologous to  Saccharomyces cerevisiae  Zap1, functions as a key regulator of zinc homeostasis and virulence in  Fusarium oxysporum , a cross‐kingdom pathogen that causes vascular wilt on more than 100 plant species and opportunistic infections in humans. Expression of  zafA  is induced under zinc‐limiting conditions and repressed by zinc. Interestingly,  zafA  is markedly up‐regulated during early stages of plant infection, suggesting that  F .  oxysporum  must cope with limited availability of zinc. Deletion of  zafA  results in deactivation of high‐affinity zinc transporters, leading to impaired growth under zinc deficiency.  Fusarium oxysporum  strains lacking ZafA are reduced in their capability to invade and kill tomato plants and the non‐vertebrate animal model  Galleria mellonella . Collectively, the results indicate that ZafA‐mediated adaptation to zinc deficiency is required for full virulence of  F .  oxysporum  on plant and animal hosts.

ZafA‐mediated regulation of zinc homeostasis is required for virulence in the plant pathogen Fusarium oxysporum