The Role of Nitric Oxide in Nitrogen Fixation by Legumes

Abstract

The legume-rhizobia symbiosis is an important process in agriculture because it allows the biological nitrogen fixation (BNF) which contributes to increasing the levels of nitrogen in the soil. Nitric oxide (•NO) is a small free radical molecule having diverse signaling roles in plants. Here we present and discuss evidence showing the role of •NO during different stages of the legume-rhizobia interaction such as recognition, infection, nodule development, and nodule senescence. Although the mechanisms by which •NO modulates this interaction are not fully understood, we discuss potential mechanisms including its interaction with cytokinin, auxin, and abscisic acid signaling pathways. In matures nodules, a more active metabolism of •NO has been reported and both the plant and rhizobia participate in •NO production and scavenging. Although •NO has been shown to induce the expression of genes coding for NITROGENASE, controlling the levels of •NO in mature nodules seems to be crucial as •NO was shown to be a potent inhibitor of NITROGENASE activity, to induce nodule senescence, and reduce nitrogen assimilation. In this sense, LEGHEMOGLOBINS (Lbs) were shown to play an important role in the scavenging of •NO and reactive nitrogen species (RNS), potentially more relevant in senescent nodules. Even though •NO can reduce NITROGENASE activity, most reports have linked •NO to positive effects on BNF. This can relate mainly to the regulation of the spatiotemporal distribution of •NO which favors some effects over others. Another plausible explanation for this observation is that the negative effect of •NO requires its direct interaction with NITROGENASE, whereas the positive effect of •NO is related to its signaling function, which results in an amplifier effect. In the near future, it would be interesting to explore the role of environmental stress-induced •NO in BNF.

The Lotus japonicus NPF3.1 Is a Nodule-Induced Gene That Plays a Positive Role in Nodule Functioning

“…The MtNPF7.6 high-affinity nitrate transporter, specifically expressed in nodule vascular tissues, functions in nitrate uptake and transport through the nodule transfer cells (NTC) to fine-tune the nodule development and functioning in response to fluctuating environmental nitrate status (Wang et al, 2020). The spatial expression profile of LjNPF3.1 in the root cortical region at the base of the nodule (Figure 2B) and in the layers of cortex adjacent to the infected cells inside the nodule (Figure 2C) is consistent with possible involvement in the flux of nitrate from the root and from outside to inside the nodule toward the N 2 -fixation zone (Figure 7) where nitrate might contribute to regulate NO homeostasis and oxidative stress (Horchani et al, 2011;Hicri et al, 2015;Valkov et al, 2017Valkov et al, , 2020Signorelli et al, 2020;Villar et al, 2020;Wang et al, 2020). However, the involvement of LjNPF3.1 should be limited to conditions of low external concentration that are permissive for nodule functioning, as the inhibitory pathway occurring at high concentrations of nitrate is not altered in the Ljnpf3.1 mutants (Figure 6B).…”

Rhizobium-Linked Nutritional and Phytochemical Changes Under Multitrophic Functional Contexts in Sustainable Food Systems

“…In return, the autotroph legumes (macrosymbionts) provide the heterotrophic Rhizobium bacteroids (microsymbionts) with organic carbon for respiration derived from photosynthetic reactions (Mitsch et al, 2018;Flores-Tinoco et al, 2020). Therefore, the root nodule is the point of convergence of two very important reactions namely, biological nitrogen fixation through nitrogenase machinery (Lindström and Mousavi, 2019;Signorelli et al, 2020), and carbon fixation in the photosynthetic machinery (Pinnola and Bassi, 2018;Vanlerberghe et al, 2020) (Figure 1). The union of Rhizobium and leguminous plants through nitrogen-fixing root nodules is an efficient nutrient cycling component in biogeochemical cycles of various ecosystems.…”

Nitrogen and Phosphorus Signaling and Transport During Legume–Rhizobium Symbiosis

“…Nitric oxide has been reported to both promote and inhibit symbiotic N fixation. These contradictory effects of NO may be associated with the level and pattern of NO production during legume–rhizobia interaction and nodule development ( Signorelli et al, 2020 ). During symbiotic interactions between L. japonicus - Mesorhizobium loti and M. truncatula - Sinorhizobium meliloti , NO was induced at 4-h postinoculation (hpi; Nagata et al, 2008 ).…”