Abstract
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.
Highlights
It is well-established that several agronomically important traits, such as plant height, grain number, and grain filling, are primarily regulated by phytohormones, such as cytokinins, gibberellins, brassinosteroids, and auxins
After verifying that the endogenous biosynthesis of Indole-3-acetic acid (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
To rule out the possibility that the changes introduced by the IAA overexpression in RD64 cells led to genetic variations that may have been selected during the initial phases of the symbiotic process, genomic DNA of both the 1021 and the RD64 bacteroids was subjected to whole genome sequencing
Summary
It is well-established that several agronomically important traits, such as plant height, grain number, and grain filling, are primarily regulated by phytohormones, such as cytokinins, gibberellins, brassinosteroids, and auxins. Carbon is assimilated during photosynthesis, while nitrogen is provided through the symbiotic fixation of atmospheric nitrogen, by the nitrogenase enzyme in rhizobial bacteroids. In these plants, the nitrogen fixation by bacteroids within root nodules and the assimilation of fixed-N into amino acids are tightly linked to carbon metabolism [4,5,6]. It is widely accepted that Rubisco, short for ribulose-1,5-biphosphate carboxylase/oxygenase, is the ultimate rate-limiting step in photosynthetic carbon fixation. Engineered plants, producing increased levels of Rubisco protein, could potentially improve CO2 fixation [9,14]. The results reported show that the expression of nitrogen-fixation genes and the activity of the nitrogenase enzyme were significantly increased in Ms-RD64 plants compared to the 1021-nodulated ones. This work highlights that the use of PGPR, triggering a balanced stimulation of C and N metabolism, could be an efficient strategy for improving plant growth
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