Dataset Information

Conditioning the soil microbiome through plant-soil feedbacks suppresses an aboveground insect pest.

ABSTRACT: Soils and their microbiomes are now recognized as key components of plant health, but how to steer those microbiomes to obtain their beneficial functions is still unknown. Here, we assess whether plant-soil feedbacks can be applied in a crop system to shape soil microbiomes that suppress herbivorous insects in above-ground tissues. We used four grass and four forb species to condition living soil. Then we inoculated those soil microbiomes into sterilized soil and grew chrysanthemum as a focal plant. We evaluated the soil microbiome in the inocula and after chrysanthemum growth, as well as plant and herbivore parameters. We show that inocula and inoculated soil in which a focal plant had grown harbor remarkably different microbiomes, with the focal plant exerting a strong negative effect on fungi, especially arbuscular mycorrhizal fungi. Soil inoculation consistently induced resistance against the thrips Frankliniella occidentalis, but not against the mite Tetranychus urticae, when compared with sterilized soil. Additionally, plant species shaped distinct microbiomes that had different effects on thrips, chlorogenic acid concentrations in leaves and plant growth. This study provides a proof-of-concept that the plant-soil feedback concept can be applied to steer soil microbiomes with the goal of inducing resistance above ground against herbivorous insects.

SUBMITTER: Pineda A

PROVIDER: S-EPMC7155073 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Conditioning the soil microbiome through plant-soil feedbacks suppresses an aboveground insect pest.

Pineda Ana A Kaplan Ian I Hannula S Emilia SE Ghanem Wadih W Bezemer T Martijn TM

The New phytologist 20200203 2

Soils and their microbiomes are now recognized as key components of plant health, but how to steer those microbiomes to obtain their beneficial functions is still unknown. Here, we assess whether plant-soil feedbacks can be applied in a crop system to shape soil microbiomes that suppress herbivorous insects in above-ground tissues. We used four grass and four forb species to condition living soil. Then we inoculated those soil microbiomes into sterilized soil and grew chrysanthemum as a focal pl ...[more]

PMID: 31863484

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Project description:Backgrounds and aimsNegative plant-soil feedbacks (PSFs) are thought to promote species coexistence, but most evidence is derived from theoretical models and data from plant monoculture experiments.MethodsWe grew Anthoxanthum odoratum and Centaurea jacea in field plots in monocultures and in mixtures with three ratios (3:1, 2:2 and 1:3) for three years. We then tested in a greenhouse experiment the performance of A. odoratum and C. jacea in pots planted with monocultures and 1:1 mixtures and filled with live and sterile soils collected from the field plots.ResultsIn the greenhouse experiment, C. jacea produced less aboveground biomass in soil conditioned by C. jacea monocultures than in soil conditioned by A. odoratum monocultures, while the aboveground biomass of A. odoratum in general did not differ between the two monospecific soils. The negative PSF effect was greater in the 1:1 plant mixture than in plant monocultures for A. odoratum but did not differ for C. jacea. In the greenhouse experiment, the performance of C. jacea relative to A. odoratum in the 1:1 plant mixture was negatively correlated to the abundance of C. jacea in the field plot where the soil was collected from. This relationship was significant both in live and sterile soils. However, there was no relationship between the performance of A. odoratum relative to C. jacea in the 1:1 plant mixture in the greenhouse experiment and the abundance of A. odoratum in the field plots.ConclusionsThe response of a plant to PSF depends on whether the focal species grows in monocultures or in mixtures and on the identity of the species. Interspecific competition can exacerbate the negative plant-soil feedbacks compared to intraspecific competition when a plant competes with a stronger interspecific competitor. Moreover, the abundance of a species in mixed plant communities, via plant-soil feedback, negatively influences the relative competitiveness of that species when it grows later in interspecific competition, but this effect varies between species. This phenomenon may contribute to the coexistence of competing plants under natural conditions through preventing the dominance of a particular plant species.

Project description:Plant-soil feedbacks (PSFs) drive plant community diversity via interactions between plants and soil microbes. However, we know little about how frequently PSFs affect plants at the seed stage, and the compositional shifts in fungi that accompany PSFs on germination.We conducted a pairwise PSF experiment to test whether seed germination was differentially impacted by conspecific versus heterospecific soils for seven grassland species. We used metagenomics to characterize shifts in fungal community composition in soils conditioned by each plant species. To investigate whether changes in the abundance of certain fungal taxa were associated with multiple PSFs, we assigned taxonomy to soil fungi and identified putative pathogens that were significantly more abundant in soils conditioned by plant species that experienced negative or positive PSFs.We observed negative, positive, and neutral PSFs on seed germination. Although conspecific and heterospecific soils for pairs with significant PSFs contained host-specialized soil fungal communities, soils with specialized microbial communities did not always lead to PSFs. The identity of host-specialized pathogens, that is, taxa uniquely present or significantly more abundant in soils conditioned by plant species experiencing negative PSFs, overlapped among plant species, while putative pathogens within a single host plant species differed depending on the identity of the heterospecific plant partner. Finally, the magnitude of feedback on germination was not related to the degree of fungal community differentiation between species pairs involved in negative PSFs. Synthesis. Our findings reveal the potential importance of PSFs at the seed stage. Although plant species developed specialized fungal communities in rhizosphere soil, pathogens were not strictly host-specific and varied not just between plant species, but according to the identity of plant partner. These results illustrate the complexity of microbe-mediated interactions between plants at different life stages that next-generation sequencing can begin to unravel.

Project description:Intraspecific negative feedback effects, where performance is reduced on soils conditioned by conspecifics, are widely documented in plant communities. However, interspecific feedbacks are less well studied, and their direction, strength, causes, and consequences are poorly understood. If more closely related species share pathogens, or have similar soil resource requirements, plants may perform better on soils conditioned by more distant phylogenetic relatives. There have been few empirical tests of this prediction across plant life stages, and none of which attempt to account for soil chemistry. Here, we test the utility of phylogeny for predicting soil feedback effects on plant survival and performance (germination, seedling survival, growth rate, biomass). We implement a full factorial experiment growing species representing five families on five plant family-specific soil sources. Our experiments exploit soils that have been cultured for over 30 years in plant family-specific beds at Oxford University Botanic Gardens. Plant responses to soil source were idiosyncratic, and species did not perform better on soils cultured by phylogenetically more distant relatives. The magnitude and sign of feedback effects could, however, be explained by differences in the chemical properties of "home" and "away" soils. Furthermore, the direction of soil chemistry-related plant-soil feedbacks was dependent on plant life stage, with the effects of soil chemistry on germination success and accumulation of biomass inversely related. Our results (1) suggest that the phylogenetic distance between plant families cannot predict plant-soil feedbacks across multiple life stages, and (2) highlight the need to consider changes in soil chemistry as an important driver of population responses. The contrasting responses at plant life stages suggest that studies focusing on brief phases in plant demography (e.g., germination success) may not give a full picture of plant-soil feedback effects.

Dataset Information

Conditioning the soil microbiome through plant-soil feedbacks suppresses an aboveground insect pest.

Publications

Conditioning the soil microbiome through plant-soil feedbacks suppresses an aboveground insect pest.

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