A Fungal Ionophore Toxin Activates Plant Inducible Immune Signaling to Promote Susceptibility

Abstract

Microbial plant pathogens deploy virulence factors to overcome host resistance or promote nutrient acquisition. Ionophores are unusual virulence factors because they activate plant immune responses through unknown pathways. The gramillin cyclic lipopeptide induces cell death and promotes virulence of Fusarium graminearum in maize but not in wheat. We demonstrate that gramillin is a virulence factor in barley spikes and Arabidopsis seedlings. Its toxicity is limited to the plant kingdom and does not require active cell metabolism. In artificial membranes, gramillin forms cation-conducting ionophores, and in leaf mesophyll cells, it causes plasma membrane depolarization and K+ leakage. Gramillin triggers plant defense responses including a ROS burst independently of MAMP receptors and dependent on ILK1, RBOHD, and BIK1. During infection, gramillin, RBOHD and ILK1 promote the expression of fungal virulence genes. We conclude that gramillin triggers host perception of ionophores to modify the host environment to favor activation of fungal pathogenesis.

Keywords: mycotoxin, virulence factor, cyclic lipopeptides, ionophore, plant immunity