Abstract

15 We investigated responses of tomato (Solanum lycopersicum) to two functional guilds of nematodes-plant parasite 16 (Meloidogyne javanica) and entomopathogens (Heterorhabditis bacteriophora, Steinernema feltiae belowground, and S. 17 carpocapsae)-as well as a leaf mining insect (Tuta absoluta) aboveground. Our results indicate that 18 entomopathogenic nematodes (EPNs): 1) induced plant defense responses, 2) reduced root knot nematode 19 (RKN) infestation belowground and 3) reduced herbivore (T. absoluta) host preference and performance 20 aboveground. Concurrently, we investigated the plant signaling mechanisms underlying these interactions using 21 biochemical and transcriptome analyses. We found that both entomopathogen and parasite triggered immune 22 responses in plant roots with shared gene expression. Tomato plants responded similarly to presence of RKN 23 or EPN in the rootzone, by rapidly activating polyphenol oxidase (PPO) and guaiacol peroxidase (GP) activity 24 in roots, but simultaneously suppressed this activity in aboveground tissues. We quantified changes in gene 25 expression in tomato that may play essential roles in defense response to RKN, which were also coincidentally 26 triggered by EPN. For example, PR-14 expression was greater in plants inoculated with EPN than in plants co-27 inoculated with both nematode functional guilds. Overall, EPN inoculation directly mediated enhanced plant 28 defense and reduced subsequent RKN infection. Likewise, we show that EPNs modulate plant defense against 29 RKN invasion, in part, by suppressing active expression of antioxidant enzymes. Inoculation of tomato roots 30 with EPNs belowground reduced both host preference and performance of the aboveground herbivore, T. 31 absoluta. Inoculations of roots with EPN also triggered an immune response in tomato via up-regulated 32 phenylpropanoid metabolism and synthesis of protease inhibitors (PIs) in plant tissues, which could explain an 33 observed decrease in egg laying and developmental performance exhibited by herbivores on EPN-inoculated 34 plants. Our results support the hypothesis that subterranean EPNs activate a battery of plant defenses 35