Involvement of Glutaredoxin and Thioredoxin Systems in the Nitrogen-Fixing Symbiosis between Legumes and Rhizobia

Abstract

Leguminous plants can form a symbiotic relationship with Rhizobium bacteria, during which plants provide bacteria with carbohydrates and an environment appropriate to their metabolism, in return for fixed atmospheric nitrogen. The symbiotic interaction leads to the formation of a new organ, the root nodule, where a coordinated differentiation of plant cells and bacteria occurs. The establishment and functioning of nitrogen-fixing symbiosis involves a redox control important for both the plant-bacteria crosstalk and the regulation of nodule metabolism. In this review, we discuss the involvement of thioredoxin and glutaredoxin systems in the two symbiotic partners during symbiosis. The crucial role of glutathione in redox balance and S-metabolism is presented. We also highlight the specific role of some thioredoxin and glutaredoxin systems in bacterial differentiation. Transcriptomics data concerning genes encoding components and targets of thioredoxin and glutaredoxin systems in connection with the developmental step of the nodule are also considered in the model system Medicago truncatula⁻Sinorhizobium meliloti.

Keywords: glutaredoxin; legume plant; redox homeostasis; stress; symbiosis; thioredoxin.

Figure 1

The indeterminate root nodule structure in Medicago truncatula. (A) Longitudinal section of indeterminate nodule 3 weeks post infection (wpi) with the apical meristem (I), the infection zone (II), and the nitrogen-fixing zone (III). (B–D) Longitudinal section of wild-type nodules 3 wpi analyzed by confocal microscopy with S. meliloti DNA stained with SYTO9 (green) and plant nuclei stained with propidium iodide (red) [8]. (C) The size of plant cells and of plant cell nuclei increases during cellular differentiation and intracellular bacterial infection occurs in zone II. (D) The nitrogen-fixing cells in zone III are fully packed with numerous elongated endosymbiotic bacteria called symbiosomes. Bars: (A) 200 µm; (B) 100 µm; (C) 10 µm; (D) 50 µm.

Figure 2

An overview of the physiological importance of Trx and Grx networks in rhizobium–legume symbiosis. Redox networks of glutaredoxin and thioredoxin systems in the two symbiotic partners is shown. The roles of (h)GSH, Grxs, and Trxs (grey squares) are indicated for bacteria (brown arrow) and for plants (green arrow). See text for details.