Aphid infestation differently affects the defences of nitrate-fed and nitrogen-fixing Medicago truncatula and alters symbiotic nitrogen fixation

Legumes can meet their nitrogen requirements through root nodule symbiosis, which could also trigger plant systemic resistance against pests. The pea aphid Acyrthosiphon pisum, a legume pest, can harbour different facultative symbionts (FS) influencing various traits of their hosts. It is therefore worth determining if and how the symbionts of the plant and the aphid modulate their interaction. We used different pea aphid lines without FS or with a single one (Hamiltonella defensa, Regiella insecticola, Serratia symbiotica) to infest Medicago truncatula plants inoculated with Sinorhizobium meliloti (symbiotic nitrogen fixation, SNF) or supplemented with nitrate (non-inoculated, NI). The growth of SNF and NI plants was reduced by aphid infestation, while aphid weight (but not survival) was lowered on SNF compared to NI plants. Aphids strongly affected the plant nitrogen fixation depending on their symbiotic status, suggesting indirect relationships between aphid- and plant-associated microbes. Finally, all aphid lines triggered expression of Pathogenesis-Related Protein 1 (PR1) and Proteinase Inhibitor (PI), respective markers for salicylic and jasmonic pathways, in SNF plants, compared to only PR1 in NI plants. We demonstrate that the plant symbiotic status influences plant–aphid interactions while that of the aphid can modulate the amplitude of the plant's defence response.