Fusaric acid-mediated S-glutathionylation of MaAKT1 channel confers the virulence of Foc TR4 to banana.

Our previous studies have demonstrated that the phytotoxin fusaric acid (FSA), secreted by several Fusarium species, acts as a key factor in the development of plant diseases; however, the underlying mechanism remains unknown. In this study, we showed that the symptoms of Fusarium wilt in banana seedlings closely resembled those observed in plants grown under potassium (K+) deficiency conditions. Mechanistically, we found that FSA induces the accumulation of intracellular reactive oxygen species (ROS), which in turn inhibits banana K+ in banana roots. This inhibition occurs via S-glutathionylation of the banana AKT1 (MaAKT1) channel, leading to reduced K+ influx and reduced K+ content in banana roots. Through mutagenesis, electrophysiological studies, immunofluorescence staining, and co-immunoprecipitation experiment, we demonstrated that mutation of Cys202, a highly conserved site in the transmembrane segment 5 of MaAKT1, diminished the biochemical interaction of glutathione (GSH) and the channel induced by FSA, and alleviated Fusarium oxysporum f. sp. cubense tropical race 4 (Foc TR4) and FSA-induced yellowing symptom. The evolutionarily conserved function of this site for S-glutathionylation was also observed in Arabidopsis AKT1 (AtAKT1) channel, as mutation of its homologue site in AtAKT1 similarly reduced the GSH-AtAKT1 interaction under FSA stress. Collectively, our results suggest that FSA contributes to disease progression by decreasing K+ absorption through S-glutathionylation of MaAKT1 channel at the conserved Cys202 residue. These findings uncover a previously unrecognized role of FSA in regulating K+ homeostasis in bananas, and provide a foundation for future strategies to treat Fusarium wilt and increase banana production by targeting the conserved S-glutathionylation site in MaAKT1 channel.