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

Abstract

Summary 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.

Soil inoculation alters the endosphere microbiome of chrysanthemum roots and leaves

“…Hence we cannot proof wich microbes present in the inoculum entered the plant. In an earlier study (Pineda et al 2020) we compared the bacterial and fungal community of soil inocula (conditioned by different species of grasses and forbs) and of sterilized soil. In that study, soil inocula have much higher bacterial and fungal richness than the sterilized soil as expected, and several bacterial phyla (Acidobacteria, Traumarcheota, Armatimonadetes, Atribacteria, BRC1, Candidatus_Berkelbacteria, Chlamydiae, Elusimicrobia, FBP, FCPU426, Fibrobacteres, Gemmatimonadetes, Hydrogenedentes, Nitrospirae, Parcubacteria, Verrucomicrobia, TM6) and a fungal phylum (Mucoromycota) were enriched in soil inocula.…”

“…Previously we observed that soil inoculation led to a reduction in thrips damage in chrysanthemum (Pineda et al 2020). Here, our objective was to examine the interactive effects of inoculation and thrips damage.…”

“…Soil from each pot was homogenized and stored individually in closed plastic bags at 4°C until used as soil inoculum in the test (feedback) phase. From previous studies, we know that conditioning field soil with grasses creates unique microbiomes that are beneficial for chrysanthemum growth (Ma et al 2017;Hannula et al 2020;Pineda et al 2020).…”

“…In our previous studies we observed that inoculating the sterilized soil with soil containing microbiomes of grass species increased the biomass of chrysanthemum when grown in presence of Pythium, a soil pathogen (Ma et al 2017(Ma et al , 2020Hannula et al 2020). Moreover, inoculation increased resistance of the plant to herbivory by thrips (Pineda et al 2020), and it suppressed negative plant-soil feedback effects on plant growth (Ma et al 2018). How soil inoculation affects the endosphere microbiome in chrysanthemum is, however, not yet known.…”

“…In previous studies our group has shown that by inoculating a background soil with a small percentage of soil that contains desired microbiomes, the soil microbiome in the background soil can be changed with cascading consequences to plant communities and even to the microbiome assembly of foliar feeding herbivore insects (Wubs et al 2016;Hannula et al 2019). Soil inoculation can also be applied to improve the health of agricultural crops as we have shown for chrysanthemum, an important horticultural cut flower crop (Ma et al 2017(Ma et al , 2020Hannula et al 2020;Pineda et al 2020). In the Netherlands this ornamental crop is grown in soil in sophisticated greenhouses, where the soil is regularly sterilized by steaming to eliminate soil borne diseases.…”