Signal interactions in pathogen and insect attack: systemic plant-mediated interactions between pathogens and herbivores of the tomato, Lycopersicon esculentum

Plant-mediated interactions (i.e., induced resistance) between plant pathogens and insect herbivores were investigated using several pests of the cultivated tomato, Lycopersicon esculentum. Single leaflets of tomato leaves were injured by allowing a third-instar Helicoverpa zea larva to feed on the leaflets or by inoculating the leaflets with Pseudomonas syringae pv. tomato (the causal agent of bacterial speck in tomato; Pst) or with Phytophthora infestans (the causal agent of late blight). Leaflets on separate plants were sprayed with benzothiadiazole, a chemical inducer of resistance to Pst. The effects of these treatments on the resistance of uninoculated or undamaged leaflets to both Pst and H. zea were then assessed after appropriate periods of time. The levels or activities of several defense-related proteins were determined in parallel. Infection of leaflets by Pst decreased the suitability of uninoculated leaflets of the same leaf for both H. zea and for Pst. Similarly, feeding by H. zea caused leaf-systemic increases in resistance to both H. zea and Pst. Infection of leaflets by P. infestans, in contrast, had no effect on resistance of leaflets to H. zea. Treatment of leaves with benzothiadiazole induced resistance to Pst but improved suitability of leaflets for H. zea. Feeding by H. zea caused the systemic accumulation of proteinase inhibitor mRNA and the systemic induction of polyphenol oxidase activity; in contrast, treatment with benzothiadiazole and inoculation with P. infestans caused the systemic accumulation of pathogenesis-related protein mRNA and the systemic induction of peroxidase activity. Inoculation of leaflets with Pst caused the leaf-systemic accumulation of both pathogenesis-related protein and proteinase inhibitor mRNA and the systemic induction of both peroxidase and polyphenol oxidase activity. These results provide clear evidence for reciprocal induced resistance involving certain pathogens and arthropod herbivores of tomato. In addition, these results provide several insights into the integration and coordination of the induced defenses of tomato against multiple pests and suggest that the expression of resistance against some pests may compromise resistance to others.