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
nematodes - plant parasite (Meloidogyne javanica) and entomopathogens
(Heterorhabditis bacteriophora, Steinernema feltiae belowground, and S.
carpocapsae) - 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. Concurrently, we
investigated the plant signaling mechanisms underlying these
interactions using biochemical and transcriptome analyses. 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 root zone, by rapidly activating
polyphenol oxidase (PPO) and guaiacol peroxidase (GP) activity in roots,
but simultaneously suppressed this activity in aboveground tissues. 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. Likewise, we show
that EPNs modulate plant defense against RKN invasion. 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 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 antagonistic effects on
temporally co-occurring subterranean plant pathogenic nematodes a