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Shoot and root insect herbivory change the plant rhizosphere microbiome and affects cabbage-insect interactions through plant-soil feedback.

ABSTRACT: Plant-soil feedback (PSF) may influence plant-insect interactions. Although plant defense differs between shoot and root tissues, few studies have examined root-feeding insect herbivores in a PSF context. We examined here how plant growth and resistance against root-feeding Delia radicum larvae was influenced by PSF. We conditioned soil with cabbage plants that were infested with herbivores that affect D. radicum through plant-mediated effects: leaf-feeding Plutella xylostella caterpillars and Brevicoryne brassicae aphids, root-feeding D. radicum larvae, and/or added rhizobacterium Pseudomonas simiae WCS417r. We analyzed the rhizosphere microbial community, and in a second set of conspecific plants exposed to conditioned soil, we assessed growth, expression of defense-related genes, and D. radicum performance. The rhizosphere microbiome differed mainly between shoot and root herbivory treatments. Addition of Pseudomonas simiae did not influence rhizosphere microbiome composition. Plant shoot biomass, gene expression, and plant resistance against D. radicum larvae was affected by PSF in a treatment-specific manner. Soil conditioning overall reduced plant shoot biomass, Pseudomonas simiae-amended soil causing the largest growth reduction. In conclusion, shoot and root insect herbivores alter the rhizosphere microbiome differently, with consequences for growth and resistance of plants subsequently exposed to conditioned soil.

SUBMITTER: Friman J

PROVIDER: S-EPMC9291931 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Insect herbivores can shift the composition of a plant community, but the mechanism underlying such shifts remains largely unexplored. A possibility is that insects alter the competitive symmetry between plant species. The effect of herbivory on competition likely depends on whether the plants are subjected to aboveground or belowground herbivory or both, and also depends on soil nitrogen levels. It is unclear how these biotic and abiotic factors interactively affect competition. In a greenhouse experiment, we measured competition between two coexisting grass species that respond differently to nitrogen deposition: Dactylis glomerata L., which is competitively favoured by nitrogen addition, and Festuca rubra L., which is competitively favoured on nitrogen-poor soils. We predicted: (1) that aboveground herbivory would reduce competitive asymmetry at high soil nitrogen by reducing the competitive advantage of D. glomerata; and (2), that belowground herbivory would relax competition at low soil nitrogen, by reducing the competitive advantage of F. rubra. Aboveground herbivory caused a 46% decrease in the competitive ability of F. rubra, and a 23% increase in that of D. glomerata, thus increasing competitive asymmetry, independently of soil nitrogen level. Belowground herbivory did not affect competitive symmetry, but the combined influence of above- and belowground herbivory was weaker than predicted from their individual effects. Belowground herbivory thus mitigated the increased competitive asymmetry caused by aboveground herbivory. D. glomerata remained competitively dominant after the cessation of aboveground herbivory, showing that the influence of herbivory continued beyond the feeding period. We showed that insect herbivory can strongly influence plant competitive interactions. In our experimental plant community, aboveground insect herbivory increased the risk of competitive exclusion of F. rubra. Belowground herbivory appeared to mitigate the influence of aboveground herbivory, and this mechanism may play a role for plant species coexistence.

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Shoot and root insect herbivory change the plant rhizosphere microbiome and affects cabbage-insect interactions through plant-soil feedback.

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