Microbial partners drive legume trait plasticity and tripartite interaction outcomes under combined stress environments

Plants often form partnerships with symbiotic microbes that improve plant performance. Increasing environmental stress is changing interaction dynamics between plants and their below-ground symbiotic partners, which can have cascading effects on above-ground trophic interactions. However, little work has examined how microbes protect plants against multiple stressors acting in concert, or the extent to which microbial genetic variation shapes context-dependent outcomes of tripartite interactions between microbes, plants, and herbivores. We experimentally manipulated the genetics of symbiotic microbial partners by individually inoculating a single legume species (Glycine max) with twenty-four genetically distinct strains of rhizobial bacteria. We quantified insect herbivore feeding and growth rates, as well as plant ecophysiological and performance traits under different combinations of drought and herbivore exposure. Rhizobial strains differentially influenced the effect of drought on legume ecophysiological traits. Certain strains increased photosynthesis and enhanced photoprotection under drought. Moreover, legumes under drought and herbivore exposure also exhibited increased photoprotection. Some strains were observed to limit herbivore growth rates under drought more effectively than others. A multivariate trait analysis revealed that strains differentially influenced legume trait syndromes and plasticity in response to stress in certain environments. Rhizobial strain variation was a key driver of tripartite interactions through changes in plant trait expression and plasticity under simultaneous abiotic and biotic stress, which had cascading effects on insect herbivore growth. A community approach incorporating multiple beneficial microbial strains may be effective for managing legume-rhizobia symbioses and introducing functional trait diversity and resistance traits into ecosystems.