Coordinate defense responses in three-way interactions between plants, insects and pathogens: Arabidopsis thaliana, Trichoplusia ni, and Pseudomonas syringae

A three-component system consisting of the cruciferous plant, Arabidopsis thaliana, the geometrid moth, Tricoplusia ni , and the bacterial pathogen Pseudomonas syringae, was used to study plant-insect-pathogen three-way interactions. I first demonstrated a trade-off between the elicitation of T. ni resistance and P. syringae resistance as a consequence of negative biochemical interactions between the jasmonic acid (JA) and salicylic acid (SA)-mediated defense signaling pathways. However, infection of avirulent P. syringae strains that typically elicit SA-regulated systemic acquired resistance, which is effective against a broad spectrum of pathogens including P. syringae , renders Arabidopsis plants more resistant to T. ni. This suggests that plants produce additional signal(s) in response to avirulent P. syringae that override the JA/SA antagonism and activate cross-protection. In contrast, virulent P. syringae strains, which do not typically induce the SA pathway, render plants systemically more susceptible, not only to subsequent attacks by T. ni but also to re-infection by the same virulent strains of P. syringae. I have called this SIS (systemic induced susceptibility). I hypothesized and subsequently demonstrated that coronatine, a phytotoxin produced by P. syringae and a mimic of JA, interferes with SA-mediated defense responses, thereby causing systemic suppression of host defenses. Importantly, I discovered that JA also induces SIS, in the same mode of action as coronatine, through the suppression of SA pathway by the activation of JA signaling pathway. In addition to its virulence function in inducing SIS in virulent infection, I found that coronatine suppresses SAR induction, probably through interfering hypersensitive responses (HR) by reinforcing the mechanism that plant use to control the extent of HR activation. The finding that avirulent P. syringae induces cross-protection against both insects and microbes provides evidence that plants evolved to activate defense response pathways against both insects and microbes simultaneously. Conversely, the coronatine-based systemic suppression of host defenses reveals a novel counter-offensive strategy employed by the pathogen.