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Volatile organic compounds emitted by the biocontrol agent Pythium oligandrum contribute to ginger plant growth and disease resistance

ABSTRACT: The oomycete Pythium oligandrum is a potential biocontrol agent to control a wide range of fungal and oomycetes-caused diseases such as Pythium myriotylum-caused rhizome rot in ginger leading to reduced yields and compromised quality. Previously, P. oligandrum has been studied for its plant growth-promoting potential by auxin production and induction of disease resistance by elicitors such as oligandrin. Volatile organic compounds (VOCs) play beneficial roles in sustainable agriculture by enhancing plant growth and resistance. We investigated the contribution of P. oligandrum-produced VOCs on plant growth and disease suppression by initially using N. benthamiana plants for screening. P. oligandrum VOCs significantly enhanced tobacco seedling and plant biomass content. Screening of the individual VOCs showed that 3-octanone and hexadecane promoted the growth of tobacco seedlings. The total VOCs from P. oligandrum also enhanced the shoot and root growth of ginger plants. Transcriptomic analysis showed a higher expression of genes related to plant growth hormones, and stress responses in the leaves of ginger plants exposed to P. oligandrum VOCs. The concentrations of plant growth hormones such as auxin, zeatin, and gibberellic acid were higher in the leaves of ginger plants exposed to P. oligandrum VOCs. In a ginger disease biocontrol assay, the VOC-exposed ginger plants infected with P. myriotylum had lower levels of disease severity. We conclude that this study contributes to understanding the growth-promoting mechanisms of P. oligandrum on ginger and tobacco, priming of ginger plants against various stress and the mechanisms of action of P. oligandrum as a biocontrol agent.

ORGANISM(S): Zingiber officinale

PROVIDER: GSE235182 | GEO | 2023/06/22

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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Volatile organic compounds emitted by the biocontrol agent Pythium oligandrum contribute to ginger plant growth and disease resistance

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