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Biological Control of Root-Knot Nematode Meloidogyne incognita Infection of Tomato (Solanum lycopersicum L.) by the Oomycete Biocontrol Agent Pythium oligandrum

ABSTRACT: The biocontrol agent Pythium oligandrum, which is a member of phylum Oomycota, can control diseases caused by a taxonomically wide range of plant pathogens, including fungi, bacteria, and oomycetes. However, whether P. oligandrum could control diseases caused by plant root-knot nematodes (RKNs) was unknown. We investigated a recently isolated P. oligandrum strain GAQ1, and the P. oligandrum CBS530.74 strain, for the control of RKN Meloidogyne incognita infection of tomato (Solanum lycopersicum L.). Initially, P. oligandrum culture filtrates were found to be lethal to M. incognita second-stage juveniles (J2s) with up to 84% mortality at 24 h after treatment compared to 14% in the control group. Consistent with the lethality to M. incognita J2s, tomato roots treated with P. oligandrum culture filtrates reduced the attraction of nematodes, and the number of nematodes penetrating the roots was reduced by up to 78%. In a greenhouse pot trial, P. oligandrum GAQ1 inoculation of tomato plants significantly reduced the gall number by 58% in plants infected with M. incognita. Notably, P. oligandrum GAQ1 mycelial treatment significantly increased tomato plant height (by 36%), weight (by 27%), and root weight (by 48%). Transcriptome analysis of tomato seedling roots inoculated with the P. oligandrum GAQ1 strain identified ~2,500 differentially expressed genes. The enriched GO terms and annotations in the up-regulated genes suggested modulation of plant hormone-signaling and defense-related pathways in response to P. oligandrum. In conclusion, our results support that P. oligandrum GAQ1 can serve as a potential biocontrol agent for M. incognita control in tomato. Multiple mechanisms appear to contribute to the biocontrol effect involving direct inhibition of M. incognita, potential priming of tomato plant defenses, and plant growth promotion.

ORGANISM(S): Solanum lycopersicum

PROVIDER: GSE262653 | GEO | 2024/04/01

REPOSITORIES: GEO

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Project description:The oomycete P. oligandrum is a soil-inhabiting parasite and predator of both fungi and oomycetes and uses hydrolytic enzymes extensively to penetrate and hydrolyze its host or prey. Other mechanisms have been overlooked, and we investigated whether P. oligandrum-produced volatile organic compounds (VOCs) could also be contributing to antagonism. VOCs have diverse functions, including contributing to antagonism in ecological interactions and potential applications in biocontrol. The growth-inhibiting activity of P. oligandrum VOCs was tested on P. myriotylum – a host or prey of P. oligandrum – coupled with electron microscopy, biochemical assays and transcriptomic analysis. The total VOCs produced by P. oligandrum reduced P. myriotylum growth by 80% and zoospore levels by 60%. GC-MS identified twenty-three VOCs, and methyl heptenone, D-limonene, 2-undecanone and 1-octanal were potent inhibitors of P. myriotylum growth and led to increased production of reactive oxygen species at a concentration that did not inhibit P. oligandrum growth. Exposure to the total VOCs of P. oligandrum led to shrinkage of P. myriotylum hyphae, and lysis of the cellular membranes and organelles. Transcriptomic analysis of P. myriotylum exposed to the P. oligandrum VOCs at increasing levels of growth inhibition showed initially a strong upregulation of putative detoxification related genes that was not maintained later during exposure to the VOCs. The inhibition of P. myriotylum growth continued after the exposure to the VOCs was discontinued and led to reduced leaf lesion size during P. myriotylum infection of its plant host. The VOCs produced by P. oligandrum could be another factor alongside hydrolytic enzymes contributing to its ecological role as a microbial antagonist where the concentration of the VOCs may be inhibitory in particular ecological niches such as in soil. The VOCs analyzed here may also be contributing to the biocontrol of diseases using P. oligandrum commercial preparations.

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