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Beneficial worm allies warn plants of parasite attack belowground and reduce aboveground herbivore preference and performance
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  • Shokoofeh Kamali,
  • Ali Javadmanesh,
  • Lukasz Stelinski,
  • Tina Kyndt,
  • Alireza seifi,
  • Monireh Cheniany,
  • Mojtaba Hosseini,
  • Mohammad Zakiaghl,
  • Mahyrar Heydarpour,
  • Javad Asili,
  • Javad Karimi
Shokoofeh Kamali
Ferdowsi University of Mashhad

Corresponding Author:shokoofeh.kamali@gmail.com

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Ali Javadmanesh
Ferdowsi University of Mashhad
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Lukasz Stelinski
University of Florida
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Tina Kyndt
Gent University
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Alireza seifi
Ferdowsi University of Mashhad
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Monireh Cheniany
Ferdowsi University of Mashhad
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Mojtaba Hosseini
Ferdowsi University of Mashhad
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Mohammad Zakiaghl
Ferdowsi University of Mashhad
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Mahyrar Heydarpour
Harvard University
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Javad Asili
Mashhad University of Medical Sciences
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Javad Karimi
Ferdowsi University of Mashhad
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1. We investigated responses of tomato (Solanum lycopersicum) to belowground presence of two functional guilds of nematodes - plant parasite (Meloidogyne javanica) and entomopathogens (Heterorhabditis bacteriophora, Steinernema feltiae, 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.
2. 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.  
3. We quantified changes in expression of candidate resistance genes in tomato that may play essential roles in defense response to RKN, which were also coincidentally triggered with 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, EPNs may modulate plant defense against RKN invasion, in part, by suppressing active expression of antioxidant enzymes.
4. 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.
5. Synthesis. Our results add to a growing body of evidence indicating that subterranean EPNs activate systemic acquired resistance (SAR) and/or induced systemic resistance (ISR) in plants with concomitant antagonistic effects on temporally co-occurring subterranean plant pathogenic nematodes and terrestrial herbivores.
30 Jun 2021Submitted to Molecular Ecology
05 Jul 2021Submission Checks Completed
05 Jul 2021Assigned to Editor
13 Jul 2021Reviewer(s) Assigned
18 Aug 2021Review(s) Completed, Editorial Evaluation Pending
15 Sep 2021Editorial Decision: Revise Minor
05 Oct 2021Review(s) Completed, Editorial Evaluation Pending
05 Oct 20211st Revision Received
18 Oct 2021Editorial Decision: Accept