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

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 addition of a microbial
inoculant increased plant biomass by ~1 standard deviation 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
application of microbial biotechnology to support sustainable agricultural
practices.