Beneficial worm allies warn plants of parasite attack belowground and reduce aboveground herbivore preference and performance

Abstract

We investigated responses of tomato to two functional guilds of\nnematodes - plant parasite (Meloidogyne javanica) and entomopathogens\n(Heterorhabditis bacteriophora, Steinernema feltiae belowground, and S.\ncarpocapsae) - as well as a leaf mining insect (Tuta absoluta)\naboveground. Our results indicate that entomopathogenic nematodes\n(EPNs): 1) induced plant defense responses, 2) reduced root knot\nnematode (RKN) infestation belowground and 3) reduced herbivore (T.\nabsoluta) host preference and performance aboveground. Concurrently, we\ninvestigated the plant signaling mechanisms underlying these\ninteractions using biochemical and transcriptome analyses. We found that\nboth entomopathogen and parasite triggered immune responses in plant\nroots with shared gene expression. Tomato plants responded similarly to\npresence of RKN or EPN in the root zone, by rapidly activating\npolyphenol oxidase (PPO) and guaiacol peroxidase (GP) activity in roots,\nbut simultaneously suppressed this activity in aboveground tissues. We\nquantified changes in gene expression in tomato that may play essential\nroles in defense response to RKN, which were also coincidentally\ntriggered by EPN. Overall, EPN inoculation directly mediated enhanced\nplant defense and reduced subsequent RKN infection. Likewise, we show\nthat EPNs modulate plant defense against RKN invasion. Inoculation of\ntomato roots with EPNs belowground reduced both host preference and\nperformance of the aboveground herbivore, T. absoluta. Inoculations of\nroots with EPN also triggered an immune response in tomato which could\nexplain an observed decrease in egg laying and developmental performance\nexhibited by herbivores on EPN-inoculated plants. Our results support\nthe hypothesis that subterranean EPNs activate a battery of plant\ndefenses associated with systemic acquired resistance (SAR) and/or\ninduced systemic resistance (ISR) with antagonistic effects on\ntemporally co-occurring subterranean plant pathogenic nematodes a