Turnabout is fair play: Maize chitinase in fall armyworm frass induces pathogen defenses in maize

Caterpillar behaviors such as feeding, crawling, and oviposition are known to induce defenses in maize and other plant species. We examined plant defense responses to another important caterpillar behavior, their defecation. Fall armyworms (FAW, Spodoptera frugiperda), a major threat to maize (Zea mays), are voracious eaters and deposit copious amounts of frass in the enclosed whorl tissue surrounding their feeding site where it remains for long periods of time. We observed that proteins from FAW frass induced a pathogenesis-related (pr) defense gene as the time after application increased. Elicitation of pathogen defenses by frass proteins was correlated with increased herbivore and reduced fungal pathogen performance over time. These responses differ from the typical plant response to oral secretions of the FAW. Fractionation of the proteins from caterpillar frass led to the identification of maize chitinases such as Pr4 that triggered pathogen-induced defenses in maize. Maize chitinases such as Pr4 are induced in plants in response to caterpillar herbivory. However, purified Pr4 protein failed to suppress growth of FAW larvae. Contrastingly, application of Pr4 on maize plants induced pathogen defenses and suppressed herbivore defenses thereby increasing the performance of the herbivores on the host. This strongly suggests that chitinases induced in maize leaves in response to caterpillar herbivory when defecated with FAW frass, acts as an effector suppressing herbivore defenses in plants.