Iturin and fengycin lipopeptides inhibit pathogenic Fusarium by targeting multiple components of the cell membrane and their regulative effects in wheat

Biocontrol microorganisms and their derived metabolites with antagonistic activity represent promising alternatives to chemical fungicides in managing plant pathogens. The lipopeptides (LPs) iturin and fengycin derived from Bacillus amyloliquefaciens S76-3 exhibit highly inhibitory effects against pathogenic fungi, especially Fusarium graminearum (Fg), the primary pathogen causing Fusarium head blight (FHB) in cereals. However, the specific target of iturin and fengycin in Fg and the underlying mechanism of antagonistic activity remain unclear. Here, global transcriptome sequencing, combined with both genetic and chemical approaches, demonstrates that the LPs exhibit antagonism toward Fg by binding to multiple components in the cell membrane of Fg cells, including ergosterol, phospholipids, glycosylphosphatidylinositol, and ankyrin. Lipopeptides result in cell swelling by inducing cell wall remodeling and osmotic substance glycerol synthesis mediated by cell wall integrity and high-osmolarity glycerol signaling pathways. Furthermore, we found that LPs can activate the induced systemic resistance in wheat against FHB and deoxynivalenol accumulation. Additionally, LPs were able to promote wheat growth by regulating auxin, cytokinin, and gibberellin signaling pathways while also delaying seed germination through the stimulation of abscisic acid and ethylene signaling pathways. These findings advance knowledge on the underlying mechanism of iturin and fengycin antagonistic activity and provide a new avenue for developing agricultural and clinical broad-spectrum antifungal agents and identifying plant growth regulators in the future.