Function of glutathione peroxidases in legume root nodules

Matamoros, Manuel A.; Saiz, Ana; Peñuelas, María; Bustos-Sanmamed, Pilar; Mulet, José; Barja, M. Victoria; Rouhier, Nicolas; Moore, Marten; James, Euan K.; Dietz, Karl‐Josef; Becana, Manuel

doi:10.1093/jxb/erv066

Cited by 44 publications

(39 citation statements)

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“…Unlike ROS, these secondary oxidation products can easily diffuse across membranes and covalently modify nuclear proteins (Farmer and Mueller, 2013). Recently, this and other laboratories have reported the presence in the nucleus of glutathione along with glutathione peroxidase and thioredoxin isoforms, supporting the importance of thiol redox signaling in this cellular compartment (Martí et al, 2009;Vivancos et al, 2010;Gaber et al, 2012;Matamoros et al, 2013Matamoros et al, , 2015. The occurrence of a variety of carbonylated proteins adds an extra layer of complexity to the redox-dependent regulation in the nucleus.…”

Section: Nuclear Proteins Are Important Targets Of Carbonylationmentioning

confidence: 59%

Protein Carbonylation and Glycation in Legume Nodules

et al. 2018

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Nitrogen fixation is an agronomically and environmentally important process catalyzed by bacterial nitrogenase within legume root nodules. These unique symbiotic organs have high metabolic rates and produce large amounts of reactive oxygen species that may modify proteins irreversibly. Here, we examined two types of oxidative posttranslational modifications of nodule proteins: carbonylation, which occurs by direct oxidation of certain amino acids or by interaction with reactive aldehydes arising from cell membrane lipid peroxides; and glycation, which results from the reaction of lysine and arginine residues with reducing sugars or their autooxidation products. We used a strategy based on the enrichment of carbonylated peptides by affinity chromatography followed by liquid chromatography-tandem mass spectrometry to identify 369 oxidized proteins in bean () nodules. Of these, 238 corresponded to plant proteins and 131 to bacterial proteins. Lipid peroxidation products induced most carbonylation sites. This study also revealed that carbonylation has major effects on two key nodule proteins. Metal-catalyzed oxidation caused the inactivation of malate dehydrogenase and the aggregation of leghemoglobin. In addition, numerous glycated proteins were identified in vivo, including three key nodule proteins: sucrose synthase, glutamine synthetase, and glutamate synthase. Label-free quantification identified 10 plant proteins and 18 bacterial proteins as age-specifically glycated. Overall, our results suggest that the selective carbonylation or glycation of crucial proteins involved in nitrogen metabolism, transcriptional regulation, and signaling may constitute a mechanism to control cell metabolism and nodule senescence.

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Section: Nuclear Proteins Are Important Targets Of Carbonylationmentioning

confidence: 59%

Protein Carbonylation and Glycation in Legume Nodules

et al. 2018

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“…2010; Matamoros et al. 2015). As growth defects in the free-living gshB mutant are rescued by exogenous GSH, it might have been expected that GSH from the plant would be able to perform the same role in symbiotic interactions.…”

Section: Discussionmentioning

confidence: 99%

“…2010; Matamoros et al. 2015). GSH biosynthesis in bacteria is a two-step process catalysed by ATP-dependent enzymes.…”

Section: Introductionmentioning

confidence: 99%

Glutathione affects the transport activity of Rhizobium leguminosarum 3841 and is essential for efficient nodulation

Cheng

Karunakaran

East

et al. 2017

FEMS Microbiology Letters

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As glutathione (GSH) plays an essential role in growth and symbiotic capacity of rhizobia, a glutathione synthetase (gshB) mutant of Rhizobium leguminosarum biovar viciae 3841 (Rlv3841) was characterised. It fails to efficiently utilise various compounds as a sole carbon source, including glucose, succinate, glutamine and histidine, and shows 60%–69% reduction in uptake rates of glucose, succinate and the non-metabolisable substrate α-amino isobutyric acid. The defect in glucose uptake can be overcome by addition of exogenous GSH, indicating GSH, but not its bacterial synthesis, is required for efficient transport. GSH is not involved in the regulation of the activity of Rlv3841's transporters via the global regulator of transport, PtsNTR. Although lack of GSH reduces transcription of the branched amino acid transporter, this was not the case for all uptake transport systems, for example, the amino acid permease. This suggests GSH alters activity and/or assembly of transport systems by an unknown mechanism. In interaction with plants, the gshB mutant is not only severely impaired in rhizosphere colonisation, but also shows a 50% reduction in dry weight of plants and nitrogen-fixation ability. This reveals that changes in GSH metabolism affect the bacterial–plant interactions required for symbiosis.

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“…In plants, there is no evidence for a PRX in the ER (Dietz, ) but recently the glutathione peroxidase‐like enzyme 3 (GPXL3) was identified as a membrane‐bound protein in the lumen of the secretory pathway of A. thaliana (Nikolovski et al ., ; Attacha et al ., ). Likewise, GPXL3 in Lotus japonicus contains a hydrophobic N‐terminal extension that may serve as a TMD and appears to be localized in the ER (Matamoros et al ., ; Attacha et al ., ). Plant GPXLs share a high sequence identity with mammalian GPXs except that they employ a cysteine rather than a selenocysteine in their active site and are reduced far more efficiently by TRX than by GSH (Navrot et al ., ).…”

Section: Formation and Isomerization Of Disulfides In The Er And The mentioning

confidence: 97%

Oxidative protein folding: state‐of‐the‐art and current avenues of research in plants

2018

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Contents Summary I. Introduction II. Formation and isomerization of disulfides in the ER and the Golgi apparatus III. The disulfide relay in the mitochondrial intermembrane space: why are plants different? IV. Disulfide bond formation on luminal proteins in thylakoids V. Conclusion Acknowledgements References SUMMARY: Disulfide bonds are post-translational modifications crucial for the structure and function of thousands of proteins. Their formation and isomerization, referred to as oxidative folding, require specific protein machineries found in oxidizing subcellular compartments, namely the endoplasmic reticulum and the associated endomembrane system, the intermembrane space of mitochondria and the thylakoid lumen of chloroplasts. At least one protein component is required for transferring electrons from substrate proteins to an acceptor that is usually molecular oxygen. For oxidation reactions, incoming reduced substrates are oxidized by thiol-oxidoreductase proteins (or domains in case of chimeric proteins), which are usually themselves oxidized by a single thiol oxidase, the enzyme generating disulfide bonds de novo. By contrast, the description of the molecular actors and pathways involved in proofreading and isomerization of misfolded proteins, which require a tightly controlled redox balance, lags behind. Herein we provide a general overview of the knowledge acquired on the systems responsible for oxidative protein folding in photosynthetic organisms, highlighting their particularities compared to other eukaryotes. Current research challenges are discussed including the importance and specificity of these oxidation systems in the context of the existence of reducing systems in the same compartments.

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Function of glutathione peroxidases in legume root nodules

Abstract: HighlightGlutathione peroxidases are antioxidant enzymes localized to different cell compartments, including the nucleus. Transcriptional and post-translational regulation via S-nitrosylation strongly suggest functions in hormonal cascades and nitric oxide redox signalling.

Cited by 44 publications

References 50 publications

Protein Carbonylation and Glycation in Legume Nodules

Protein Carbonylation and Glycation in Legume Nodules

Glutathione affects the transport activity of Rhizobium leguminosarum 3841 and is essential for efficient nodulation

Oxidative protein folding: state‐of‐the‐art and current avenues of research in plants

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