Negative hormonal regulation of symbiotic nodule development. I. Ethylene (review)

The process of symbiotic nodule formation resulting from interaction between legume plants and rhizobia is controlled by both partners. From the plant side the important role belongs to a system of hormonal regulation, involving all classes of phytohormones identified in plants. Negative regulation of nodulation is very important for the plant since the symbiotic nodule formation is highly energy-consuming process. Moreover, nodules lacking nitrogen fixation might be formed during interaction with ineffective strain of rhizobia, and it is disadvantageous for the plant. Up to now, there are data about involving of four phytohormones into negative regulation of nodule formation: ethylene, abscisic, jasmonic and salicylic acids. In this review, the role of ethylene in negative regulation of nodulation is discussed. Ethylene negatively regulates the number of developing symbiotic nodules at different stages of their formation. The first negative effect of ethylene appears at the level of calcium spiking, triggered by Nod-factors produced by rhizobia. Further, ethylene negatively influences deformations of roots hairs, stimulated by Nod-factors, infection thread growth, as well as nodule primordium development. In tropical legume Sesbania rostrata Bremek. & Oberm. ethylene represses the activity of nodule meristem, leading to formation of determinate type of nodule (with temporal meristem activity), while at the absence of ethylene indeterminate nodules (with prolonged meristem activity) are formed. At the same time, it was found that in soybean Glycine max (L.) Merr., ethylene is not involved in regulation of nodulation. It seems that ethylene involvement into regulation of nodule formation is not strictly dependent on the type of nodules, since in the other legume plants, forming determinate nodules, number of nodules is negatively affected by ethylene. It is suggested that ethylene synthesis in inoculated roots is triggered by Nod-factors, which activate plant defense responses, leading to restriction of number of forming nodules. Hypernodulating mutant of Medicago truncatula Gaertn. sickle, carrying a mutation in the gene MtEIN2, which is the key component in ethylene signal transduction pathway, is characterized by decreased level of defense response activation, as it was shown by proteomic analysis. It is interesting that not only the plants, but rhizobia as well can control ethylene level in rhizosphere and therefore influence nodule number. One of such mechanisms is the synthesis of rhizobitoxin by some rhizobial strains, which has structural similarity with inhibitor of ethylene synthesis aminoethoxyvinilglycine (AVG). The other mechanism is more widespread among rhizobia and it deals with synthesis of ACC deaminase, an enzyme, which cleaves the precursor of ethylene synthesis 1-aminocyclopropane-1-carboxylic acid (ACC). Thus, regulation of ethylene level may be important for practical application, potentially allowing to increase plant's ability to nodulation. However, it should be taken into account that nodule number is precisely regulated by the plant because nodule formation is very energy-consuming process. Even more, it is necessary to remember that ethylene stimulates development of root hairs and decrease of their level may influence an intake ability of root and lead to deficiency of nutrient elements.