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Mol Ecol

Title:		Beneficial worm allies warn plants of parasite attack below-ground and reduce above-ground herbivore preference and performance
Author(s):		Kamali S; Javadmanesh A; Stelinski LL; Kyndt T; Seifi A; Cheniany M; Zaki-Aghl M; Hosseini M; Heydarpour M; Asili J; Karimi J;
Address:		"Department of Plant Protection, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran. Department of Animal Science, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran. Department of Entomology and Nematology, University of Florida Citrus Research and Education Center, Lake Alfred, Florida, USA. Department of Molecular Biotechnology, Ghent University, Ghent, Belgium. Department of Biotechnology and Plant Breeding, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran. Department of Biology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, Iran. Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA. Department of Pharmacognosy, School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran"
Journal Title:		Mol Ecol
Year:		2022
Volume:		20211115
Issue:		2
Page Number:		691 - 712
DOI:		10.1111/mec.16254
ISSN/ISBN:		1365-294X (Electronic) 0962-1083 (Linking)
Abstract:		"Antagonistic interactions among different functional guilds of nematodes have been recognized for quite some time, but the underlying explanatory mechanisms are unclear. We investigated responses of tomato (Solanum lycopersicum) to two functional guilds of nematodes-plant parasite (Meloidogyne javanica) and entomopathogens (Heterorhabditis bacteriophora, Steinernema feltiae below-ground, and S. carpocapsae)-as well as a leaf mining insect (Tuta absoluta) above-ground. Our results indicate that entomopathogenic nematodes (EPNs): (1) reduced root knot nematode (RKN) infestation below-ground, (2) reduced herbivore (T. absoluta) host preference and performance above-ground, and (3) induced overlapping plant defence responses by rapidly activating polyphenol oxidase and guaiacol peroxidase activity in roots, but simultaneously suppressing this activity in above-ground tissues. Concurrently, we investigated potential plant signalling mechanisms underlying these interactions using transcriptome analyses. We found that both entomopathogens and plant parasites triggered immune responses in plant roots with shared gene expression. Secondary metabolite transcripts induced in response to the two nematode functional guilds were generally overlapping and showed an analogous profile of regulation. Likewise, we show that EPNs modulate plant defence against RKN invasion, in part, by suppressing active expression of antioxidant enzymes. Inoculations of roots with EPN triggered an immune response in tomato via upregulated phenylpropanoid metabolism and synthesis of protease inhibitors in plant tissues, which may explain decreased egg laying and developmental performance exhibited by herbivores on EPN-inoculated plants. Furthermore, changes induced in the volatile organic compound-related transcriptome indicated that M. javanica and/or S. carpocapsae inoculation of plants triggered both direct and indirect defences. Our results support the hypothesis that plants 'mistake' subterranean EPNs for parasites, and these otherwise beneficial worms activate a battery of plant defences associated with systemic acquired resistance and/or induced systemic resistance with concomitant antagonistic effects on temporally co-occurring subterranean plant pathogenic nematodes and terrestrial herbivores"
Keywords:		Animals Herbivory *Solanum lycopersicum/genetics *Parasites Plant Roots *Tylenchoidea Meloidogyne javanica Tuta absoluta EPN-induced plant defence biological control entomopathogenic nematodes molecular ecology multitrophic interactions phenylpropanoid bi;
Notes:		"MedlineKamali, Shokoofeh Javadmanesh, Ali Stelinski, Lukasz L Kyndt, Tina Seifi, Alireza Cheniany, Monireh Zaki-Aghl, Mohammad Hosseini, Mojtaba Heydarpour, Mahyar Asili, Javad Karimi, Javad eng p3/35682/Ferdowsi University of Mashhad/ Research Support, Non-U.S. Gov't England 2021/10/28 Mol Ecol. 2022 Jan; 31(2):691-712. doi: 10.1111/mec.16254. Epub 2021 Nov 15"