Jasmonic and salicylic acid pathways shape the rhizosphere microbiome, affecting aphid herbivory and soil-mediated insect-plant interactions in a density-dependent manner.

Abstract

Aboveground induction of plant defense pathways can shape root-associated microbial communities. However, whether these changes are pathway-specific and how they affect plant growth and resistance remain unclear. We evaluated how induction of the jasmonic acid (JA) and salicylic acid (SA) defense pathways shapes the root microbiome of Brassica oleracea and whether these soil-mediated shifts affect plant growth and resistance to herbivory in a subsequent generation using a plant-soil feedback approach. In the conditioning phase, defense pathways were induced either through foliar application of methyl jasmonate and SA solutions or through herbivory by caterpillars (JA) and aphids (SA). Both pathways led to distinct shifts in microbial communities, with the bacterial and fungal composition varying by pathway identity and induction method. JA induction resulted in more differentially abundant amplicon sequence variants than SA induction, particularly with Proteobacteria depletion. Conversely, Planctomycetota (bacteria) and Mortierellomycota (fungi) were enriched under both pathways, suggesting that these represent general stress-responsive groups. In the feedback phase, JA- and SA-conditioned soils had no effect on resistance under high aphid pressure, whereas under low aphid density, plants grown in SA-conditioned soil exhibited reduced phloem feeding and lower aphid population development. Together, our results indicate that the benefits provided by the defense-shaped root microbiome depend on pest pressure intensity and arise from overall community shifts rather than specific taxa enrichment. Our findings underscore the complex interactions between plant defense pathways, rhizosphere microbes, and herbivores.