Salicylate-mediated interactions between pathogens and herbivores

Plants employ hormone-mediated signaling pathways to defend against pathogens and insects. We tested predictions about the relative effect of jasmonate and salicylate pathways and how they mediate interactions between pathogens and herbivores. We employed two pathogens of tomato, Pseudomonas syringae (Pst) and tobacco mosaic virus (TMV), that are known to elicit distinct components of the two pathways, and we address the consequences of their induction for resistance in wild-type and salicylate-deficient transgenic plants in field experiments. We report that Pst infection induced jasmonic acid and proteinase inhibitors (PIs), and reduced the growth of Spodoptera exigua caterpillars on wild-type and salicylate-deficient plants. Pst and TMV both induced salicylic acid in wild-type but not salicylate-deficient plants. Although TMV did not affect jasmonic acid or PIs, infection increased caterpillar growth on wild-type plants, but not on salicylate-deficient plants. Aphid population growth was higher on salicylate-deficient compared to wild-type plants, and lower on salicylate-induced plants compared to controls. Natural aphid colonization was reduced on TMV-infected wild types, but not on salicylate-deficient plants. In sum, jasmonate-mediated resistance is induced by some pathogens, independent of salicylate, and salicylate-mediated induction by other pathogens results in induced susceptibility to a chewer and resistance to an aphid. We conclude with a predictive model for the expression of defense pathways and their consequences.