Combined effects of mutualistic rhizobacteria counteract virus-induced suppression of indirect plant defenses in soybean

It is increasingly clear that microbial plant symbionts can influence interactions between their plant hosts and other organisms. Yet, such effects remain poorly understood, particularly under ecologically realistic conditions where plants simultaneously interact with diverse mutualists and antagonists. Here we examine how the effects of a plant virus on indirect plant defenses against its insect vector are influenced by co-occurrence of other microbial plant symbionts. Using a multi-factorial design, we manipulated colonization of soybean using three different microbes: a pathogenic plant virus (Bean pod mottle virus [BPMV]), a nodule-forming beneficial rhizobacterium (Bradyrhizobium japonicum), and a plant growth-promoting rhizobacterium (PGPR) (Delftia acidovorans). We then assessed recruitment of parasitoids (Pediobious foveolatus [Eulophidae]) and parasitism rates following feeding by the BPMV vector Epilachna varivestis (Coccinellidae). BPMV infection suppressed parasitoid recruitment, prolonged parasitoid foraging time, and reduced parasitism rates in semi-natural foraging assays. However, simultaneous colonization of BPMV-infected hosts by both rhizobacteria restored parasitoid recruitment and rates of parasitism to levels similar to uninfected controls. Co-colonization by the two rhizobacteria also enhanced parasitoid recruitment in the absence of BPMV infection. These results illustrate the potential of plant-associated microbes to influence indirect plant defenses, with implications for disease transmission and herbivory, but also highlight the potential complexity of such interactions.