Pea aphid promotes amino acid metabolism both in Medicago truncatula and bacteriocytes to favor aphid population growth under elevated CO2

Rising atmospheric CO2 levels can dilute the nitrogen (N) resource in plant tissue, which is disadvantageous to many herbivorous insects. Aphids appear to be an exception that warrants further study. The effects of elevated CO2 (750ppm vs. 390ppm) were evaluated on N assimilation and transamination by two Medicago truncatula genotypes, a N-fixing-deficient mutant (dnf1) and its wild-type control (Jemalong), with and without pea aphid (Acyrthosiphon pisum) infestation. Elevated CO2 increased population abundance and feeding efficiency of aphids fed on Jemalong, but reduced those on dnf1. Without aphid infestation, elevated CO2 increased photosynthetic rate, chlorophyll content, nodule number, biomass, and pod number for Jemalong, but only increased pod number and chlorophyll content for dnf1. Furthermore, aphid infested Jemalong plants had enhanced activities of N assimilation-related enzymes (glutamine synthetase, Glutamate synthase) and transamination-related enzymes (glutamate oxalate transaminase, glutamine phenylpyruvate transaminase), which presumably increased amino acid concentration in leaves and phloem sap under elevated CO2. In contrast, aphid infested dnf1 plants had decreased activities of N assimilation-related enzymes and transmination-related enzymes and amino acid concentrations under elevated CO2. Furthermore, elevated CO2 up-regulated expression of genes relevant to amino acid metabolism in bacteriocytes of aphids associated with Jemalong, but down-regulated those associated with dnf1. Our results suggest that pea aphids actively elicit host responses that promote amino acid metabolism in both the host plant and in its bacteriocytes to favor the population growth of the aphid under elevated CO2.