Spatiotemporal patterns of induced resistance and susceptibility linking diverse plant parasites

Abstract

Induced defenses mediate interactions between parasites sharing the same host plant, but the outcomes of these interactions are challenging to predict because of spatiotemporal variation in plant responses and differences in defense pathways elicited by herbivores or pathogens. Dissecting these mediating factors necessitates an approach that encompasses a diversity of parasitic feeding styles and tracks interactions over space and time. We tested indirect plant-mediated relationships across three tomato (Solanum lycopersicum) consumers: (1) the fungal pathogen-powdery mildew, Oidium neolycopersici; (2) a sap-feeding insect-silverleaf whitefly, Bemisia tabaci; and (3) a chewing insect-the leaf miner, Tuta absoluta. Further, we evaluated insect/pathogen responses on local vs. systemic leaves and over short (1 day) vs. long (4 days) time scales. Overall, we documented: (1) a bi-directional negative effect between O. neolycopersici and B. tabaci; (2) an asymmetrical negative effect of B. tabaci on T. absoluta; and (3) an asymmetrical positive effect of T. absoluta on O. neolycopersici. Spatiotemporal patterns varied depending on the species pair (e.g., whitefly effects on leaf miner performance were highly localized to the induced leaf, whereas effects on pathogen growth were both local and systemic). These results highlight the context-dependent effects of induced defenses on a diverse community of tomato parasites. Notably, the outcomes correspond to those predicted by phytohormonal theory based on feeding guild differences with key implications for the recent European invasion by T. absoluta.