Sharon E. Zytynska

To cope with abiotic and biotic stressors, plants have developed mutualistic associations with beneficial soil microbes, but little is known about how extreme abiotic conditions impact on microbe‐induce resistance to insect herbivores. Extreme temperatures are often accompanied by extremes in plant water availability, which together reduce plant growth and change plant physiology. There are potential consequences for increasing plant susceptibility to biotic stresses, and this poses a real challenge for plant productivity. We evaluated how the effects of beneficial soil bacteria ( Acidovorax radicis N35e) on barley plant growth and resultant resistance against aphid infestation ( Sitobion avenae ) were impacted by a single heatwave event across a plant water availability gradient. We also tested if timing of bacterial inoculation (before or after the temperature treatment) affected bacteria‐plant interactions on aphids. We found that heatwaves affected plant biomass allocation from above‐ground to below‐ground tissues. Inoculation with A. radicis led to reduction of aphid numbers, but depended on timing of inoculation, and led to stronger resistance when inoculations occurred closer to aphid infestation. Remarkably, microbe‐induced resistance against aphids was consistent across heatwave and water availability treatments. This study provides evidence that beneficial plant‐bacteria interactions may represent a potential solution for sustainable agricultural practices to enhance plant growth and response to insect pests under climate change. Future field trials should investigate the consistency of beneficial effects reported here for a better understanding of multispecies interactions in the context of global change. Read the free Plain Language Summary for this article on the Journal blog.

Plants and insect herbivores are two of the most diverse multicellular groups in the world, and both are strongly influenced by interactions with the belowground soil microbiome. Effects of reciprocal rapid evolution on ecological interactions between herbivores and plants have been repeatedly demonstrated, but it is unknown if (and how) the soil microbiome could mediate these eco‐evolutionary processes on a shared host plant. We tested the role of a plant‐beneficial soil bacterium Acidovorax radicis in altering eco‐evolutionary interactions between different aphid genotypes ( Sitobion avenae , genotypes Sickte and Fescue) feeding on barley Hordeum vulgare . We measured fecundity, longevity and population growth of two aphid genotypes reared separately or together (population mixture) on three different barley varieties that were inoculated with or without A. radicis . Results showed that across all plant varieties A. radicis increased plant growth and suppressed aphid populations via reduced longevity and fecundity. The strength of effect was dependent on aphid genotype and barley variety, while the direction of effect was altered by aphid population mixture. Using Lotka–Volterra modelling, we demonstrated that while A. radicis inoculation decreased growth rates for both aphid genotypes it increased the competitiveness of one genotype against the other. In general, in the presence of A. radicis , the Fescue aphid genotype became more inhibitory of Sickte aphids, while Sickte aphids facilitated the growth of Fescue aphids. Our work demonstrates that plant rhizosphere microbiomes exert community‐level influences by mediating eco‐evolutionary interactions between herbivores and host plants. By altering competitive interaction outcomes among aphids and thus impacting processes such as rapid evolution, soil microbes contribute to the short‐ and long‐term structure and functioning of terrestrial habitats.