Involvement of Glutaredoxin and Thioredoxin Systems in the Nitrogen-Fixing Symbiosis between Legumes and Rhizobia Geneviève Alloing, Karine Mandon, Eric Boncompagni, Françoise Montrichard, Pierre Frendo To cite this version: Geneviève Alloing, Karine Mandon, Eric Boncompagni, Françoise Montrichard, Pierre Frendo. In- volvement of Glutaredoxin and Thioredoxin Systems in the Nitrogen-Fixing Symbiosis between Legumes and Rhizobia. Antioxidants , MDPI, 2018, 7 (12), pp.182. 10.3390/antiox7120182. hal- 02138466 HAL Id: hal-02138466 https://hal.archives-ouvertes.fr/hal-02138466 Submitted on 26 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. antioxidants Review Involvement of Glutaredoxin and Thioredoxin Systems in the Nitrogen-Fixing Symbiosis between Legumes and Rhizobia Geneviève Alloing 1, Karine Mandon 1, Eric Boncompagni 1, Françoise Montrichard 2 and Pierre Frendo 1,* 1 Université Côte d’Azur, INRA, CNRS, ISA, France; [email protected] (G.A.); [email protected] (K.M.); [email protected] (E.B.) 2 IRHS, INRA, AGROCAMPUS-Ouest, Université d’Angers, SFR 4207 QUASAV, 42 rue Georges Morel, 49071 Beaucouzé CEDEX, France; [email protected] * Correspondence: [email protected] Received: 29 October 2018; Accepted: 1 December 2018; Published: 5 December 2018 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: thioredoxin; glutaredoxin; legume plant; symbiosis; redox homeostasis; stress 1. Introduction Most terrestrial plants establish symbiotic relationships with fungi or bacteria that provide nutrients for their growth [1,2]. Nitrogen and phosphorous are critical determinants of plant growth and productivity. Amongst the plant families, leguminous plants can achieve a nitrogen-fixing symbiosis with soil bacteria of the family Rhizobiaceae to reduce atmospheric nitrogen (N2) to ammonia [3]. The ability to reduce N2 is restricted to bacteria and archaea which produce the enzyme nitrogenase. Legumes are an economically important plant family, for their contribution to animal and human nutrition on one hand, and for their ecosystemic services in cropping systems on the other hand, by participating to nitrogen enrichment of soils and thereby to a reduced use of nitrogen fertilizers. The study of these symbioses is therefore a major challenge to promote a more environmentally-friendly agriculture. The nitrogen-fixing symbiosis (NFS) between rhizobia bacteria and legumes leads to the formation of new root organs, called nodules [4,5]. The development of the nodule requires many crucial steps to achieve the fixation of atmospheric nitrogen. The first step is the cross recognition between bacteria and the plant partner. This recognition involves the nodulation (Nod) factors produced by the bacteria that play a major role in the symbiotic specificity between the two partners. In parallel to bacterial recognition, Nod factors promote the development of a new meristem in the plant root that leads to the Antioxidants 2018, 7, 182; doi:10.3390/antiox7120182 www.mdpi.com/journal/antioxidants Antioxidants 2018, 7, 182 2 of 17 establishment of the root nodule. Subsequently, the formation of infection threads allows the transport of bacteriaAntioxidants from 2018 the, 7 surface, x FOR PEER of theREVIEW root to the plant cells that will host bacteria, in an endosymbiotic2 of 17 way. The accommodation of numerous bacteria inside plant cells and nitrogen fixation requirements involve plant root that leads to the establishment of the root nodule. Subsequently, the formation of infection modificationsthreads allows of the the cellular transport structure of bacteria and from physiology the surface of bothof the partners root to the for plant maintaining cells that will the symbiotichost interaction.bacteria, These in an modifications endosymbiotic areway. achieved The accommodation through differentiation of numerous bacteria of the plant inside cells plant which cells and includes cell enlargement,nitrogen fixation DNA requirements endoreduplication, involve modifications and significant of the cellular reprogramming structure and of physiology cellular structure of both and metabolismpartners [6 ].for Cellularmaintaining and the biochemical symbiotic changesinteraction. are These also modifications observed during are achieved the differentiation through of differentiation of the plant cells which includes cell enlargement, DNA endoreduplication, and bacteria into N2-fixing bacteroids. Amongst them, a high aerobic metabolism provides ATP and reductantssignificant necessary reprogramming to sustain nitrogenaseof cellular structure activity, whereasand metabolism the nitrogen-fixing [6]. Cellular enzymeand biochemical is irreversibly changes are also observed during the differentiation of bacteria into N2-fixing bacteroids. Amongst inactivated by oxygen. Thus nitrogen-fixation efficiency depends on oxygen protective mechanisms them, a high aerobic metabolism provides ATP and reductants necessary to sustain nitrogenase involvingactivity, the formationwhereas the of nitrogen-fixing an oxygen barrier enzyme cell is layerirreversibly around inactivated the infected by oxygen. cells and Thus the nitrogen- production of a symbioticfixation hemoglobin, efficiency depends called on leghemoglobin. oxygen protective This mechanisms later is involved involving in the the formation protection of an of oxygen nitrogenase from denaturation,barrier cell layer and around in the the supply infected of cells ample and amountthe production of oxygen of a symbiotic to bacteria hemoglobin, for respiration. called The supplyleghemoglobin. of energy from This the later plant is involved to nitrogen-fixing in the protection bacteroids, of nitrogenase and thefrom export denaturation, of ammonia and in the from the bacteroidssupply to of the ample roots amount also requireof oxygen major to bacteria metabolic for respiration. adaptations The supply in the nodules.of energy from In conclusion, the plant the noduleto functioningnitrogen-fixing depends bacteroids, on and a strict the export regulation of ammo ofnia the from development the bacteroids and to the roots metabolism also require of plant major metabolic adaptations in the nodules. In conclusion, the nodule functioning depends on a strict and bacteria cells. regulation of the development and the metabolism of plant and bacteria cells. The nodulesThe nodules are consideredare considered as as “indeterminate” “indeterminate” or or “determinate” “determinate” according according to their to theirmode modeof of developmentdevelopment [7]. [7]. In theIn the determinate determinate nodules, nodules, such as as those those of of soybean soybean (Glycine (Glycine max), max the), nodular the nodular meristemsmeristems are transientlyare transiently active. active. This This results results inin sphericalspherical nodules, nodules, containi containingng cells cellswith witha similar a similar developmentaldevelopmental state state to each to each other. other. In In the the indeterminate indeterminate nodules, nodules, such such as those as those formed formed by pea by (Pisum pea ( Pisum sativumsativum), alfalfa), alfalfa (Medicago (Medicago sativa sativa) or) barrelor barrel medic medic (M. (M. truncatula truncatula),), thethe meristemsmeristems persist persist throughout throughout the plant’sthe life, plant’s giving life, an giving elongated an elongated nodule. nodule. Consequently, Consequently, the functionalthe functional nodule nodule presents presents three three zones: zones: (I) the meristematic zone, (II) the infection zone, and (III) the N2-fixing zone (Figure 1A,B). At (I) the meristematic zone, (II) the infection zone, and (III) the N -fixing zone (Figure1A,B). At later later stage, there is a rupture in the symbiotic interaction, which occurs2 in the senescence zone (zone stage, there is a rupture in the symbiotic interaction, which occurs in the senescence zone (zone IV). IV). FigureFigure 1. The 1. indeterminateThe