DOI: 10.5061/dryad.x0k6djhjs
title: Beneficial worm allies warn plants of parasite attack belowground and reduce aboveground herbivore preference and performance

description: We investigated responses of tomato (Solanum lycopersicum) 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 rootzone, 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. For
 example, PR-14 expression was greater in plants inoculated with EPN than
 in plants co-inoculated with both nematode functional guilds. Overall, EPN
 inoculation directly mediated enhanced plant defense and reduced
 subsequent RKN infection. Likewise, we show that EPNs modulate plant
 defense against RKN invasion, in part, by suppressing active expression of
 antioxidant enzymes. 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.
description: Results
 from three different experiments are presented here: Experiment 1.
 Interactions between the root-knot nematode, <i>M.
 javanica</i> and entomopathogenic nematodes, <i>H.
 bacteriophora</i>, <i>S. feltiae</i>, and <i>S.
 carpocapsae. </i> Experiment 2.
 Response of <i>T. absoluta</i> females to tomato plants
 inoculated with RKN or EPN . Experiment 3.
 Gene expression in tomato exposed to RKN, EPN, or leafminer
 herbivory.
description: The folder named DATA includes 2 files:MOL ECOL Data is an excel
 file including 7 sheets. These sheets represent data from the following
 experiments : Nematode infection experiments, two sheets for Estimation of
 defense-related enzyme activity (GP and PPO), Two-choice assays, No
 Choice, herbivore developmental stage, and No-choice assays.
 Javad-Karimi_DATA_Readme has details and explanations of variables and
 data within the excel sheet.