Plant and Aphid Genotypes Modulate Legume Rhizobium-Induced Defense Against Aphids

Sustainable protein production is needed to ensure food security while mitigating climate change. Leguminous crops contribute to these goals by providing protein-rich seeds and improving soil fertility through nitrogen-fixing symbiosis (NFS) with rhizobia. Beyond their nutritional and agronomic benefits, legumes face major challenges from insect herbivores such as the pea aphid, Acyrthosiphon pisum. While NFS can enhance plant defences against aphids, the influence of plant and aphid genotypic variation on these rhizobia-mediated effects remains poorly understood. Here, we investigated how genotype interactions influence rhizobia-mediated defence priming by using two Medicago truncatula genotypes (A17 and R108) grown under NFS with Sinorhizobium meliloti 2011 or nitrate (NI) feeding conditions and infested with three clonal lines representing two pea aphid biotypes. We analysed aphid performance, plant fitness, and plant leaf expression of defence genes associated with the jasmonic acid (JA) and salicylic acid (SA) signalling pathways over a 12-day period following aphid infestation. Aphid fitness varied significantly with both plant and aphid genotypes and was further modulated by rhizobia inoculation. Expression of defence marker genes involved in SA and JA pathway was dependent on specific plant-aphid genotype combinations and was significantly modulated by rhizobia inoculation. This pattern suggests that both SA- and JA-mediated plant defences contribute to regulating aphid weight, possibly through different mechanisms or in response to different plant-aphid interactions. Our study shows that plant and aphid genotypes, rhizobia inoculation and interactions (G x G x R) are thus central components driving plantaphid-rhizobia interaction dynamics. Our study highlights importance of genetic context and microbial symbiosis in structuring multitrophic interactions and suggests new opportunities to optimize pest resistance using plant-beneficial microbial associations.