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

Citation

Kamali, Shokoofeh et al. (2021), Beneficial worm allies warn plants of parasite attack belowground and reduce aboveground herbivore preference and performance, Dryad, Dataset, https://doi.org/10.5061/dryad.x0k6djhjs

Abstract

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.

Methods

Results from three different experiments are presented here:

Experiment 1. Interactions between the root-knot nematode, M. javanica and entomopathogenic nematodes, H. bacteriophora, S. feltiae, and S. carpocapsae.

Experiment 2. Response of T. absoluta females to tomato plants inoculated with RKN or EPN .

Experiment 3. Gene expression in tomato exposed to RKN, EPN, or leafminer herbivory.

Usage Notes

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.

Funding

Ferdowsi University of Mashhad, Award: p3/ 43844