Contrasting effects of native soil microbiomes on direct and indirect herbivore resistance in a dominant shrub species

Abstract Background and Aims The soil microbiome is known to modulate plant resistance to insect herbivores. Research on this topic has traditionally focused on bottom-up effects of plants on insects (direct resistance). However, how soil microbiomes affect plant resistance via top-down control of insects by natural enemies (indirect resistance) remains understudied. We conducted a greenhouse experiment using Baccharis salicifolia as a model to test the effects of native soil microbiomes on (i) direct resistance against the generalist aphid Aphis gossypii and (ii) indirect resistance by natural enemies. Methods We grew B. salicifolia plants in a common sterilized substrate that was either inoculated with 10% native field soil or left uninoculated as a sterile control and performed a bioassay with A. gossypii to assess direct resistance by measuring aphid performance (age at first reproduction and reproductive rate). Then, we assessed indirect resistance by excluding natural enemies and estimating effects on aphid colony size in plants growing in inoculated vs. uninoculated soil. Key Results Plants in inoculated soil exhibited a 15% increase in growth, while aphid reproduction was reduced by 18% compared to uninoculated soil. Moreover, soil inoculation significantly altered the strength of top-down control by natural enemies. Access to natural enemies reduced aphid colony size by 23% in uninoculated soils but only by 11% in inoculated soils, indicating weaker indirect resistance under soil inoculation. Conclusions We show that native microbial communities regulate plant-insect-natural enemy interactions via contrasting effects on direct and indirect resistance, underscoring the need to consider both pathways to understand microbial impacts on plant resistance.