N-terminal acetyltransferase complex FonNatA acetylates transcriptional factor FonMeaB to regulate the pathogenicity of Fusarium oxysporum f. sp. niveum on watermelon.

N-terminal acetyltransferase (NAT) complexes play key roles in various biological processes; however, their functions and mechanisms in plant pathogenic fungi remain poorly understood. This study explores the roles of FonNAT complexes in Fusarium oxysporum f. sp. niveum (Fon), the causal agent of watermelon Fusarium wilt. Fon possesses five FonNAT complexes with unique roles in vegetative growth, conidiation, conidial morphology, and stress responses. Disrupting FonNaa10 and FonNaa15, encoding for the catalytic and auxiliary subunits of the FonNatA complex, compromised the ability of Fon to penetrate host tissues, reducing fungal invasive growth and pathogenicity. FonNaa10 exhibited N-terminal acetyltransferase activity dependent on FonNaa15 and interacted with the bZIP transcription factor FonMeaB, which binds to the novel cis-element BSMN (CATCATCATCA) in FonNmr promoters. Acetylation at lysine 69 catalyzed by FonNaa10 stabilized FonMeaB under preferential nitrogen source, ammonium nitrate, suppressing downstream FonNmr gene expression. Conversely, lack of acetylation under a secondary nitrogen source, sodium nitrate, destabilized FonMeaB, leading to upregulation of FonNmr genes. The FonNatA complex plays a critical role in the pathogenicity of Fon through the site-specific acetylation of lysine residues in FonMeaB. This work offers insights into how nitrogen source-dependent acetylation modulates Fon pathogenicity, providing new strategies for controlling plant fungal diseases.