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

Alloing, Geneviève; Mandon, Karine; Boncompagni, Éric; Montrichard, Françoise; Frendo, Pierre

doi:10.3390/antiox7120182

Cited by 20 publications

(14 citation statements)

References 99 publications

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“…These working conditions involve a specific cellular redox control in both symbiotic partners. The contribution of reactive oxygen and N species (ROS and RNS) and the importance of the antioxidant defence in the formation and the functioning of root nodules have been largely demonstrated (Alloing et al, 2018;Damiani et al, 2016;Frendo et al, 2013;Puppo et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Legume nodule senescence: a coordinated death mechanism between bacteria and plant cells

Kazmierczak

Boncompagni

et al. 2020

Advances in Botanical Research

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In the legume-rhizobia symbiosis, atmospheric dinitrogen (N 2 ) fixation by rhizobia takes place in a specific root organ, called the nodule. During biological N 2 fixation, the plant provides photosynthetic carbohydrates to bacteria and, in exchange, bacteria feed the plant with reduced nitrogen (N) under ammonia (NH 3 ) form. Like most other organs, the root nodule has a limited lifespan, and eventually enters a senescence process characterized by a decline of N 2 fixation and the coordinated death of both bacteria and plant cells. This senescence process characterized by a metabolic switch from a carbon sink to a nutrient source either results from nodule aging (developmental nodule senescence) or can be triggered prematurely by adverse environmental conditions. Accumulating evidence suggests that redox and hormone signaling contribute to the triggering of senescence. Indeed, nodule senescence is a developmentally programmed process in which antioxidants, reactive oxygen and N species (ROS/RNS), hormones and proteinases play key roles. This chapter reviews recent knowledge on nodule senescence and proposes models by which ROS, RNS, and likely hormones intervene in the orchestration of this process.

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Section: Introductionmentioning

confidence: 99%

Legume nodule senescence: a coordinated death mechanism between bacteria and plant cells

Kazmierczak

Boncompagni

et al. 2020

Advances in Botanical Research

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“…caulinodans and other rhizobia must be able to withstand oxidative stress in the host environment to establish successful symbiotic relationships with the host plants. At the first encounter with S. rostrata, A. caulinodans is recognised as an invader and triggers an oxidative burst [11,18,67]. OHPs are produced by host plants as a part of the defence response against bacterial infection, and subsequently react with free fatty acids and cell membranes, leading to the production of other organic radicals, which increases their toxicity [26].…”

Section: Discussionmentioning

confidence: 99%

Ohr and OhrR Are Critical for Organic Peroxide Resistance and Symbiosis in Azorhizobium caulinodans ORS571

Guo

Deng

et al. 2020

Genes

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Azorhizobium caulinodans is a symbiotic nitrogen-fixing bacterium that forms both root and stem nodules on Sesbania rostrata. During nodule formation, bacteria have to withstand organic peroxides that are produced by plant. Previous studies have elaborated on resistance to these oxygen radicals in several bacteria; however, to the best of our knowledge, none have investigated this process in A. caulinodans. In this study, we identified and characterised the organic hydroperoxide resistance gene ohr (AZC_2977) and its regulator ohrR (AZC_3555) in A. caulinodans ORS571. Hypersensitivity to organic hydroperoxide was observed in an ohr mutant. While using a lacZ-based reporter system, we revealed that OhrR repressed the expression of ohr. Moreover, electrophoretic mobility shift assays demonstrated that OhrR regulated ohr by direct binding to its promoter region. We showed that this binding was prevented by OhrR oxidation under aerobic conditions, which promoted OhrR dimerization and the activation of ohr. Furthermore, we showed that one of the two conserved cysteine residues in OhrR, Cys11, was critical for the sensitivity to organic hydroperoxides. Plant assays revealed that the inactivation of Ohr decreased the number of stem nodules and nitrogenase activity. Our data demonstrated that Ohr and OhrR are required for protecting A. caulinodans from organic hydroperoxide stress and play an important role in the interaction of the bacterium with plants. The results that were obtained in our study suggested that a thiol-based switch in A. caulinodans might sense host organic peroxide signals and enhance symbiosis.

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“…In the absence of functional DNF1, the NCRs that were tested by the authors were found to be trapped inside the endoplasmic reticulum, effectively blocking bacteroid differentiation [16]. It has been found that different plant-and bacteria-derived thioredoxin (Trx) and glutaredoxin (Grx) systems are necessary for nitrogen-fixing symbiosis (reviewed in [35]). For example, one plant-derived thioredoxin (Trx-s1) has been found to be induced in the nodule infection zone and to interact with several NCR peptides.…”

Section: Ncrs Primarily But Not Only Act As Mediators Of Terminal Bmentioning

confidence: 99%

Symbiotic Outcome Modified by the Diversification from 7 to over 700 Nodule-Specific Cysteine-Rich Peptides

Roy

Achom

Wilkinson

et al. 2020

Genes

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Legume-rhizobium symbiosis represents one of the most successfully co-evolved mutualisms. Within nodules, the bacterial cells undergo distinct metabolic and morphological changes and differentiate into nitrogen-fixing bacteroids. Legumes in the inverted repeat lacking clade (IRLC) employ an array of defensin-like small secreted peptides (SSPs), known as nodule-specific cysteine-rich (NCR) peptides, to regulate bacteroid differentiation and activity. While most NCRs exhibit bactericidal effects in vitro, studies confirm that inside nodules they target the bacterial cell cycle and other cellular pathways to control and extend rhizobial differentiation into an irreversible (or terminal) state where the host gains control over bacteroids. While NCRs are well established as positive regulators of effective symbiosis, more recent findings also suggest that NCRs affect partner compatibility. The extent of bacterial differentiation has been linked to species-specific size and complexity of the NCR gene family that varies even among closely related species, suggesting a more recent origin of NCRs followed by rapid expansion in certain species. NCRs have diversified functionally, as well as in their expression patterns and responsiveness, likely driving further functional specialisation. In this review, we evaluate the functions of NCR peptides and their role as a driving force underlying the outcome of rhizobial symbiosis, where the plant is able to determine the outcome of rhizobial interaction in a temporal and spatial manner.

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

Cited by 20 publications

References 99 publications

Legume nodule senescence: a coordinated death mechanism between bacteria and plant cells

Legume nodule senescence: a coordinated death mechanism between bacteria and plant cells

Ohr and OhrR Are Critical for Organic Peroxide Resistance and Symbiosis in Azorhizobium caulinodans ORS571

Symbiotic Outcome Modified by the Diversification from 7 to over 700 Nodule-Specific Cysteine-Rich Peptides

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