Root microbes can improve plant tolerance to insect damage: A systematic review and meta‐analysis

Abstract

To limit damage from insect herbivores, plants rely on a blend of defensive mechanisms that includes partnerships with beneficial microbes, particularly those inhabiting roots. While ample evidence exists for microbially mediated resistance responses that directly target insects through changing phytotoxin and volatile profiles, we know surprisingly little about the microbial underpinnings of plant tolerance. Tolerance defenses counteract insect damage via shifts in plant physiology that reallocate resources to fuel compensatory growth, improve photosynthetic efficiency, and reduce oxidative stress. Despite being a powerful mitigator of insect damage, tolerance remains an understudied realm of plant defenses. Here, we propose a novel conceptual framework that can be broadly applied across study systems to characterize microbial impacts on expression of tolerance defenses. We conducted a systematic review of studies quantifying the impact of rhizosphere microbial inoculants on plant tolerance to herbivory based on several measures—biomass, oxidative stress mitigation, or photosynthesis. We identified 40 studies, most of which focused on chewing herbivores (n = 31) and plant growth parameters (e.g., biomass). Next, we performed a meta‐analysis investigating the impact of microbial inoculants on plant tolerance to herbivory, which was measured via differences in plant biomass, and compared across key microbe, insect, and plant traits. Thirty‐five papers comprising 113 observations were included in this meta‐analysis, with effect sizes (Hedges' d) ranging from −4.67 (susceptible) to 18.38 (overcompensation). Overall, microbial inoculants significantly reduce the cost of herbivory via plant growth promotion, with overcompensation and compensation comprising 25% of observations of microbial‐mediated tolerance. The grand mean effect size 0.99 [0.49; 1.49] indicates that the addition of a microbial inoculant increased plant biomass by ~1 SD under herbivore stress, thus improving tolerance. This effect was influenced most by microbial attributes, including functional guild and total soil community diversity. Overall, results highlight the need for additional investigation of microbially mediated plant tolerance, particularly in sap‐feeding insects and across a more comprehensive range of tolerance mechanisms. Such attention would round out our current understanding of anti‐herbivore plant defenses, offer insight into the underlying mechanisms that promote resilience to insect stress, and inform the application of microbial biotechnology to support sustainable agricultural practices.