Plant Pathogens Moonlighting as Beneficial Insect Symbionts

Herbivorous insects can shape the epidemiology of disease in plants by vectoring numerous phytopathogens. While the consequences of infection are often well-characterized in the host plant, the extent to which phytopathogens alter the physiology and development of their insect vectors remains poorly understood. In this review, we highlight how insect-borne phytopathogens can promote vector fitness, consistent with theoretical predictions that selection should favor a mutualistic or commensal phenotype. In doing so, we define the metabolic features predisposing plant pathogens to engage in beneficial partnerships with herbivorous insects and how these mutualisms promote the microbe's propagation to uninfected plants. For the vector, the benefits of co-opting microbial pathways and metabolites can be immense: from balancing a nutritionally deficient diet and unlocking a novel ecological niche to upgrading its defensive biochemistry against natural enemies. Given the independent origins of these tripartite interactions and a number of convergent features, we also discuss the evolutionary and genomic signatures underlying microbial adaptation to its dual lifestyle as both a plant pathogen and an insect mutualist. Finally, as host association can constrain the metabolic potential of microbes over evolutionary time, we outline the stability of these interactions and how they impact the virulence and transmission of plant pathogens.