Aphid infestation differently affects the defences of nitrate-fed and nitrogenfixing 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 marker 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.