Indole-3-acetic acid (IAA) is the main auxin acting as a phytohormone in many plant developmental processes. The ability to synthesize IAA is widely associated with plant growth-promoting rhizobacteria (PGPR). Several studies have been published on the potential application of PGPR to improve plant growth through the enhancement of their main metabolic processes. In this study, the IAA-overproducing Ensifer meliloti strain RD64 and its parental strain 1021 were used to inoculate Medicago sativa plants. After verifying that the endogenous biosynthesis of IAA did not lead to genomic changes during the initial phases of the symbiotic process, we analyzed whether the overproduction of bacterial IAA inside root nodules influenced, in a coordinated manner, the activity of the nitrogen-fixing apparatus and the photosynthetic function, which are the two processes playing a key role in legume plant growth and productivity. Higher nitrogen-fixing activity and a greater amount of total nitrogen (N), carbon (C), Rubisco, nitrogen-rich amino acids, soluble sugars, and organic acids were measured for RD64-nodulated plants compared to the plants nodulated by the wild-type strain 1021. Furthermore, the RD64-nodulated plants showed a biomass increase over time, with the highest increment (more than 60%) being reached at six weeks after infection. Our findings show that the RD64-nodulated plants need more substrate derived from photosynthesis to generate the ATP required for their increased nitrogenase activity. This high carbohydrate demand further stimulates the photosynthetic function with the production of molecules that can be used to promote plant growth. We thus speculate that the use of PGPR able to stimulate both C and N metabolism with a balanced C/N ratio represents an efficient strategy to obtain substantial gains in plant productivity.
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