Cross-regulation of Fusarium mycotoxin production through activation of plant stress signaling

The Fusarium graminearum fungus produces secondary metabolite virulence factors during plant infection to scavenge nutrients in the apoplastic space and overcome host defenses. We recently identified a cyclic lipopeptide produced by Fusarium graminearum called gramillin which is a virulence factor in maize silks but not in wheat spikes. Gramillin is toxic to maize but not to wheat cells, though the mechanism for gramillin toxicity is unknown. Our work indicates that gramillin targets plant membranes which it disrupts ion homeostasis causing necrosis and cell death. In artificial membranes, gramillin functions as a cation-conducting ionophore, and in leaf mesophyll cells, gramillin causes plasma membrane depolarization and K+ leakage. Gramillin’s toxic effect on plant membranes extends across monocots and dicots where it also induces cellular stress responses including a ROS burst which is dependent on RBOHD and ILK1 host genes. During infection, gramillin suppresses host defensive barrier formation and promotes fungal expression of secondary metabolite biosynthetic genes. These processes require the RBOHD and ILK1 genes which promote susceptibility. We conclude that gramillin targets plant membrane responses to promote susceptibility to the F. graminearum fungal pathogen.