Plants engage in beneficial plant microbe interactions with rhizobia and with arbuscular mycorrhizal fungi to increase their uptake of nutrients, such as nitrogen, phosphate, and potassium from soils. In exchange for these nutrients, the plant invests a significant proportion of its photosynthetically fixed carbon in these interactions. To be beneficial for the host, the nutrient benefits must outweigh the carbon costs of the symbiosis for the host. To reduce carbon costs, the host plant must be able to distinguish between low or high benefit symbionts and must invest its carbon resources strategically. We examined the physiological and molecular responses in nitrogen deficient plants that were colonized with low or high benefit partners, or that were simultaneously colonized with low or high benefit partners in split root experiments. We found that higher benefits in nitrogen and phosphate uptake by the arbuscular mycorrhizal symbiosis are linked to an elevated expression of strigolactone biosynthesis, and mycorrhiza-induced phosphate, ammonium and nitrate transporters. Plant nutrient demand but also fungal access to nitrogen played an important role for the carbon transport to different root symbionts in tripartite interactions, and the plant allocated more carbon to rhizobia under nitrogen demand, but more carbon to the fungal partner, when the fungal partner had access to nitrogen. Legumes punish non-nitrogen fixing rhizobia with reduced carbon supply, but the time point of nodulation by high or low benefit partners plays an important role for the carbon costs of these non-beneficial interactions and the molecular responses in plants.