D3296: The role of a below-ground natural enemy in inducing host plant resistance during the interaction between above-below ground herbivores

We investigated the responses of tomato to two functional guilds of nematodes - plant parasite (Meloidogyne javanica) and entomopathogens belowground - as well as a leaf mining insect (Tuta absoluta) aboveground. Our results indicate that entomopathogenic nematodes (EPNs): 1) induced plant defense responses, 2) reduced root knot nematode (RKN) infestation belowground and 3) reduced herbivore (T. absoluta) host preference and performance aboveground. We found that both entomopathogen and parasite triggered immune responses in plant roots with shared gene expression. Tomato plants responded similarly to presence of RKN or EPN in the rootzone, by rapidly activating polyphenol oxidase (PPO) and guaiacol peroxidase (GPX) activity in roots. We quantified changes in gene expression in tomato that may play essential roles in defense response to RKN, which were also coincidentally triggered by EPN. Overall, EPN inoculation directly mediated enhanced plant defense and reduced subsequent RKN infection. Inoculation of tomato roots with EPNs belowground reduced both host preference and performance of the aboveground herbivore, T. absoluta.  Inoculations of roots with EPN also triggered an immune response in tomato via up-regulated phenylpropanoid metabolism and synthesis of protease inhibitors (PIs) in plant tissues, which could explain an observed decrease in egg laying and developmental performance exhibited by herbivores on EPN-inoculated plants. Our results support the hypothesis that subterranean EPNs activate a battery of plant defenses associated with systemic acquired resistance (SAR) and/or induced systemic resistance (ISR) with concomitant antagonistic effects on temporally co-occurring subterranean plant pathogenic nematodes and terrestrial herbivores.