Microbes Attaching to Endoparasitic Phytonematodes in Soil Trigger Plant Defense Upon Root Penetration by the Nematode

Abstract

Root-knot nematodes (Meloidogyne spp.) are among the most aggressive phytonematodes. While moving through soil to reach the roots of their host, specific microbes attach to the cuticle of the infective second-stage juveniles (J2). Reportedly, the attached microorganisms affect nematodes and reduce their performance on the host plants. We have previously shown that some non-parasitic bacterial strains isolated from the cuticle of Meloidogyne hapla in different soils affected J2 mortality, motility, hatching, and root invasion. Here we tested whether cuticle-attached microbes trigger plant defenses upon penetration of J2. In in vitro assays, M. hapla J2-attached microbes from a suppressive soil induced pathogenassociated molecular pattern-triggered immunity (PTI) in tomato roots. All tested PTIresponsive defense genes were upregulated after root invasion of J2 with attached microbes, compared to surface-sterilized J2, particularly the jasmonic acid-mediated PTI marker genes TFT1 and GRAS4.1. The strain Microbacterium sp. K6, that was isolated from the cuticle, significantly reduced root invasion when attached to the J2. Attached K6 cells supported plant defense and counteracted suppression of plant basal defense in roots by invaded J2. The plant response to the J2-attached K6 cells was stronger in leaves than in roots, and it increased from 1 to 3 days post inoculation (dpi). At 1 dpi, the plant responded to J2-attached K6 cells by ameliorating the J2-triggered down-regulation of defense genes mostly in roots, while at 3 dpi this response was systemic and more pronounced in leaves. In a reactive oxygen species (ROS) assay, the compounds released from J2 with attached K6 cells triggered a stronger ROS burst in tomato roots than the compounds from nematodes without K6, or the metabolites released from strain K6 alone. Leaves showed a 100 times more sensitive response than roots, and the metabolites of K6 with or without J2 induced strong ROS bursts. In conclusion, our results suggest the importance of microorganisms that attach to M. hapla in suppressive soil, inducing early basal defenses in plants and suppressing nematode performance in roots.

Bacterial Community Structure Dynamics in Meloidogyne incognita -Infected Roots and Its Role in Worm-Microbiome Interactions

“…This could be an artifact of the Baermann tray method, but the evidence supporting J2's active attraction to this isolate could point to a more elaborate form of interaction in which the bacterium first attracts the nematode to hitchhike into the root and, once established, can help guide the nematode into less abstracted sections of the root. Evidence of bacterial J2 hitchhikers, which perform some function inside the root, has been presented in the past (64). However, these bacteria were RKN pathogens that also elicited ROS production, a plant defense mechanism.…”

Plants and Associated Soil Microbiota Cooperatively Suppress Plant-Parasitic Nematodes

“…(Giné et al, 2016) Bulk soil Flavobacterium,Chryseobacterium,Flexibacter,Steroidobacter,Methylobacterium,Fusarium,Preussia,Ctenomyces,Mortierella,Cladosporium,Stachybotrys,Pseudallescheria,Psathyrella,Heydenia Heterodera glycines (Hamid et al, 2017) Rhizosphere ITS -amplicon Mortierella, Purpureocillium, Fusarium, Pochonia, Clonostachys, Scleroderma, Penicillium, Aspergillus, Corynespora, Guehomyces, Humicola, Eupenicillium, Cryptococcus, Monographella, Tetracladium, Geomyces, Stachybotrys, Ilyonectria, Myrothecium, Monodictys, Arthrobotrys, Dactylellina, Drechslerella, Haptocillium, Hirsutella, Trichoderma, Acremonium, Penicillium, Nematoctonus, Catenaria (Continued) against M. hapla, but a combination of a direct antagonism and induced resistance provided a better protection to the plants. They also showed in a sterile system that the microbes attaching to the cuticle of M. hapla in the suppressive soil induced systemic resistance in the plant upon nematode invasion (Topalović et al, 2020a). In addition, in recent years scientists have intensively explored the role of plant and microbial volatile organic compounds on nematode parasitism (Huang et al, 2010;Yang et al, 2012;Barros et al, 2014;Xu et al, 2015;Estupiñan-López et al, 2018;Silva et al, 2018;Pedroso et al, 2019).…”

“…On the other hand, some endoparasitic nematodes, like Meloidogyne spp., hide from the strong plant defense responses by moving through the apoplast until reaching permanent feeding sites (Sijmons et al, 1991;Williamson and Hussey, 1996;Shah et al, 2017). It was recently shown that microorganisms attaching to the J2 of M. hapla in suppressive soil before J2 penetration into the roots increase their recognition by the plant by upregulating several PTI-responsive defense genes (Topalović et al, 2020a). Studying the microbially induced chemical and metabolic changes in nematode perception by the plant would better elucidate the exact mechanisms in this tripartite interaction.…”

Plants Specifically Modulate the Microbiome of Root-lesion Nematodes in the Rhizosphere, Affecting Their Fitness

“…While searching for a suitable host or surviving adverse conditions, these nematodes migrate through soil where they are exposed to a vast variety of microorganisms. Depending on the nature of plant-nematodemicrobe interactions in soil, plants may be protected by specific mutualistic microbes [3][4][5]. The term "holobiont" defines a macroorganism (plant or animal) as a unit that includes all its associated (micro)organisms [6,7].…”

“…There is a specific microbial attachment to phytonematodes in soil that is dependent on the nematode species and the soil type [16,17]. It was suggested that, besides directly antagonizing their nematode carriers, nematode-attached microbes can trigger plant defense responses against nematode attack [3]. The surface coat (SC) is the outermost glycoprotein layer that covers the nematode cuticle [17].…”