Characteristics and Research Progress of Legume Nodule Senescence

Delaying the nodule senescence of legume crops can prolong the time of nitrogen fixation and attenuate the lack of fertilizer in the later stage of legume crop cultivation, resulting in improved crop yield and reduced usage of nitrogen fertilizer. However, effective measures to delay the nodule senescence of legume crops in agriculture are relatively lacking. In the present review, we summarized the structural and physiological characteristics of nodule senescence, as well as the corresponding detection methods, providing technical support for the identification of nodule senescence phenotype. We then outlined the key genes currently known to be involved in the regulation of nodule senescence, offering the molecular genetic information for breeding varieties with delayed nodule senescence. In addition, we reviewed various abiotic factors affecting nodule senescence, providing a theoretical basis for the interaction between molecular genetics and abiotic factors in the regulation of nodule senescence. Finally, we briefly prospected research foci of nodule senescence in the future.

NO Network for Plant–Microbe Communication Underground: A Review

Mechanisms governing plant–microbe interaction in the rhizosphere attracted a lot of investigative attention in the last decade. The rhizosphere is not simply a source of nutrients and support for the plants; it is rather an ecosystem teeming with diverse flora and fauna including different groups of microbes that are useful as well as harmful for the plants. Plant–microbe interaction occurs via a highly complex communication network that involves sophisticated machinery for the recognition of friend and foe at both sides. On the other hand, nitric oxide (NO) is a key, signaling molecule involved in plant development and defense. Studies on legume–rhizobia symbiosis suggest the involvement of NO during recognition, root hair curling, development of infection threads, nodule development, and nodule senescence. A similar role of NO is also suggested in the case of plant interaction with the mycorrhizal fungi. Another, insight into the plant–microbe interaction in the rhizosphere comes from the recognition of pathogen-associated molecular patterns (PAMPs)/microbe-associated molecular patterns (MAMPs) by the host plant and thereby NO-mediated activation of the defense signaling cascade. Thus, NO plays a major role in mediating the communication between plants and microbes in the rhizosphere. Interestingly, reports suggesting the role of silicon in increasing the number of nodules, enhancing nitrogen fixation, and also the combined effect of silicon and NO may indicate a possibility of their interaction in mediating microbial communication underground. However, the exact role of NO in mediating plant–microbe interaction remains elusive. Therefore, understanding the role of NO in underground plant physiology is very important, especially in relation to the plant’s interaction with the rhizospheric microbiome. This will help devise new strategies for protection against phytopathogens and enhancing plant productivity by promoting symbiotic interaction. This review focuses on the role of NO in plant–microbe communication underground.

The Fungicide Tetramethylthiuram Disulfide Negatively Affects Plant Cell Walls, Infection Thread Walls, and Symbiosomes in Pea (Pisum sativum L.) Symbiotic Nodules

In Russia, tetramethylthiuram disulfide (TMTD) is a fungicide widely used in the cultivation of legumes, including the pea (Pisum sativum). Application of TMTD can negatively affect nodulation; nevertheless, its effect on the histological and ultrastructural organization of nodules has not previously been investigated. In this study, the effect of TMTD at three concentrations (0.4, 4, and 8 g/kg) on nodule development in three pea genotypes (laboratory lines Sprint-2 and SGE, and cultivar ‘Finale’) was examined. In SGE, TMTD at 0.4 g/kg reduced the nodule number and shoot and root fresh weights. Treatment with TMTD at 8 g/kg changed the nodule color from pink to green, indicative of nodule senescence. Light and transmission electron microscopy analyses revealed negative effects of TMTD on nodule structure in each genotype. ‘Finale’ was the most sensitive cultivar to TMTD and Sprint-2 was the most tolerant. The negative effects of TMTD on nodules included the appearance of a senescence zone, starch accumulation, swelling of cell walls accompanied by a loss of electron density, thickening of the infection thread walls, symbiosome fusion, and bacteroid degradation. These results demonstrate how TMTD adversely affects nodules in the pea and will be useful for developing strategies to optimize fungicide use on legume crops.

Responses of mature symbiotic nodules to the whole-plant systemic nitrogen signaling

In symbiotic root nodules of legumes, terminally differentiated rhizobia fix atmospheric N2 producing an NH4+ influx that is assimilated by the plant. The plant, in return, provides photosynthates that fuel the symbiotic nitrogen acquisition. Mechanisms responsible for the adjustment of the symbiotic capacity to the plant N demand remain poorly understood. We have investigated the role of systemic signaling of whole-plant N demand on the mature N2-fixing nodules of the model symbiotic association Medicago truncatula/Sinorhizobium using split-root systems. The whole-plant N-satiety signaling rapidly triggers reductions of both N2 fixation and allocation of sugars to the nodule. These responses are associated with the induction of nodule senescence and the activation of plant defenses against microbes, as well as variations in sugars transport and nodule metabolism. The whole-plant N-deficit responses mirror these changes: a rapid increase of sucrose allocation in response to N-deficit is associated with a stimulation of nodule functioning and development resulting in nodule expansion in the long term. Physiological, transcriptomic, and metabolomic data together provide evidence for strong integration of symbiotic nodules into whole-plant nitrogen demand by systemic signaling and suggest roles for sugar allocation and hormones in the signaling mechanisms.

Nitric oxide signaling, metabolism and toxicity in nitrogen-fixing symbiosis

Interactions between legumes and rhizobia lead to the establishment of a symbiotic relationship characterized by the formation of a new organ, the nodule, which facilitates the fixation of atmospheric nitrogen (N2) by nitrogenase through the creation of a hypoxic environment. Significant amounts of nitric oxide (NO) accumulate at different stages of nodule development, suggesting that NO performs specific signaling and/or metabolic functions during symbiosis. NO, which regulates nodule gene expression, accumulates to high levels in hypoxic nodules. NO accumulation is considered to assist energy metabolism within the hypoxic environment of the nodule via a phytoglobin–NO-mediated respiration process. NO is a potent inhibitor of the activity of nitrogenase and other plant and bacterial enzymes, acting as a developmental signal in the induction of nodule senescence. Hence, key questions concern the relative importance of the signaling and metabolic functions of NO versus its toxic action and how NO levels are regulated to be compatible with nitrogen fixation functions. This review analyses these paradoxical roles of NO at various stages of symbiosis, and highlights the role of plant phytoglobins and bacterial hemoproteins in the control of NO accumulation.