Limited impact of elevated levels of polyphenol oxidase on tree-feeding caterpillars: assessing individual plant defenses with transgenic poplar

Abstract

Polyphenol oxidase (PPO) is commonly believed to function as an effective antiherbivore defense in plants. PPO is induced in plants following herbivory, and insect performance is often negatively correlated with PPO levels. However, induced defenses create numerous changes in plants, and very little work has been done to test the direct effects of PPO on insect herbivores separately from other changes. This study examined the impacts of high levels of PPO on the performance of two species of tree-feeding caterpillars (Lymantria dispar and Orgyia leucostigma) on poplar. Transgenic PPO-overexpressing poplar (Populus tremula x Populus alba) was used as a source of elevated-PPO leaves, thereby controlling for the multiple effects of induction. In addition, the impacts of treating poplar foliage with high levels of purified mushroom PPO were examined on the two caterpillar species. Contrary to expectation, in several cases increased PPO levels had no significant effect on insect consumption or growth rates. Although one of the mechanisms by which PPO is believed to impact herbivores is via increased oxidative stress, the ingestion of large amounts of PPO had little or no effect on semiquinone radical and oxidized protein levels in the gut contents of lymantriid caterpillars. PPO activity in caterpillars is likely limited by the low oxygen and high ascorbate levels commonly found in their gut contents. This study questions whether induced PPO functions as an effective post-ingestive defense against tree-feeding caterpillars, and indicates that controlled, mechanistic studies are needed in other plant-herbivore systems to test for a direct effect of PPO on insect performance.