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

Abstract

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.