Diverse Genetic Mechanisms Enable Pseudomonas syringae to Rapidly Overcome Effector-Triggered Immunity

Bacterial plant pathogens pose a serious threat to worldwide crop yields and cause widespread food insecurity. One common approach to limit pathogen proliferation on critical crops is to genetically engineer cultivars that harbour resistance genes capable of recognising and responding to critical bacterial virulence factors like type III secreted effectors. Unfortunately, these resistance barriers are often overcome by pathogen evolution within just a few seasons. In this study, we explore the evolutionary mechanisms that enable pathogens to overcome plant resistance by leveraging two Pseudomonas syringae pv. maculicola strains that differ in their ability to cause disease on the model host Arabidopsis thaliana. We first characterise the molecular basis of the adaptation that enabled the P. syringae pv. maculicola PmaES4326 to overcome rps5-mediated resistance through a direct modification to its hopAR1 effector. We then show that through in planta evolution, the initially nonpathogenic strain P. syringae pv. maculicola PmaYM7930 can rapidly adapt to overcome rps5-mediated resistance via low-frequency mutations that do not involve direct modifications to hopAR1. This result was especially surprising because hopAR1 is known to be associated with mobile genetic elements that enable increased evolutionary plasticity. The rapid ability of P. syringae to overcome effector-triggered immunity without direct modifications to hopAR1 reveals that the genetic mechanisms enabling pathogens to overcome host resistance are more diverse than is currently recognised. This result has important implications for the development of more stably resistant crops that can resist various forms of pathogen evolution.