Function of glutathione peroxidases in legume root nodules

Matamoros MA, Saiz A, Peñuelas M, Bustos-Sanmamed P, Mulet JM, Barja MV, Rouhier N, Moore M, James EK, Dietz K-J, Becana M (2015)
Journal of Experimental Botany 66(10): 2979-2990.

Zeitschriftenaufsatz | Veröffentlicht| Englisch
 
Download
Es wurde kein Volltext hochgeladen. Nur Publikationsnachweis!
Autor/in
Matamoros, Manuel A.; Saiz, Ana; Peñuelas, Maria; Bustos-Sanmamed, Pilar; Mulet, Jose M.; Barja, Maria V.; Rouhier, Nicolas; Moore, MartenUniBi; James, Euan K.; Dietz, Karl-JosefUniBi; Becana, Manuel
Abstract / Bemerkung
Glutathione peroxidases (Gpxs) are antioxidant enzymes not studied so far in legume nodules, despite the fact that reactive oxygen species are produced at different steps of the symbiosis. The function of two Gpxs that are highly expressed in nodules of the model legume Lotus japonicus was examined. Gene expression analysis, enzymatic and nitrosylation assays, yeast cell complementation, in situ mRNA hybridization, immunoelectron microscopy, and LjGpx-green fluorescent protein (GFP) fusions were used to characterize the enzymes and to localize each transcript and isoform in nodules. The LjGpx1 and LjGpx3 genes encode thioredoxin-dependent phospholipid hydroperoxidases and are differentially regulated in response to nitric oxide (NO) and hormones. LjGpx1 and LjGpx3 are nitrosylated in vitro or in plants treated with S-nitrosoglutathione (GSNO). Consistent with the modification of the peroxidatic cysteine of LjGpx3, in vitro assays demonstrated that this modification results in enzyme inhibition. The enzymes are highly expressed in the infected zone, but the LjGpx3 mRNA is also detected in the cortex and vascular bundles. LjGpx1 is localized to the plastids and nuclei, and LjGpx3 to the cytosol and endoplasmic reticulum. Based on yeast complementation experiments, both enzymes protect against oxidative stress, salt stress, and membrane damage. It is concluded that both LjGpxs perform major antioxidative functions in nodules, preventing lipid peroxidation and other oxidative processes at different subcellular sites of vascular and infected cells. The enzymes are probably involved in hormone and NO signalling, and may be regulated through nitrosylation of the peroxidatic cysteine essential for catalytic function.
Erscheinungsjahr
2015
Zeitschriftentitel
Journal of Experimental Botany
Band
66
Ausgabe
10
Seite(n)
2979-2990
ISSN
1460-2431
Page URI
https://pub.uni-bielefeld.de/record/2737383

Zitieren

Matamoros MA, Saiz A, Peñuelas M, et al. Function of glutathione peroxidases in legume root nodules. Journal of Experimental Botany. 2015;66(10):2979-2990.
Matamoros, M. A., Saiz, A., Peñuelas, M., Bustos-Sanmamed, P., Mulet, J. M., Barja, M. V., Rouhier, N., et al. (2015). Function of glutathione peroxidases in legume root nodules. Journal of Experimental Botany, 66(10), 2979-2990. doi:10.1093/jxb/erv066
Matamoros, M. A., Saiz, A., Peñuelas, M., Bustos-Sanmamed, P., Mulet, J. M., Barja, M. V., Rouhier, N., Moore, M., James, E. K., Dietz, K. - J., et al. (2015). Function of glutathione peroxidases in legume root nodules. Journal of Experimental Botany 66, 2979-2990.
Matamoros, M.A., et al., 2015. Function of glutathione peroxidases in legume root nodules. Journal of Experimental Botany, 66(10), p 2979-2990.
M.A. Matamoros, et al., “Function of glutathione peroxidases in legume root nodules”, Journal of Experimental Botany, vol. 66, 2015, pp. 2979-2990.
Matamoros, M.A., Saiz, A., Peñuelas, M., Bustos-Sanmamed, P., Mulet, J.M., Barja, M.V., Rouhier, N., Moore, M., James, E.K., Dietz, K.-J., Becana, M.: Function of glutathione peroxidases in legume root nodules. Journal of Experimental Botany. 66, 2979-2990 (2015).
Matamoros, Manuel A., Saiz, Ana, Peñuelas, Maria, Bustos-Sanmamed, Pilar, Mulet, Jose M., Barja, Maria V., Rouhier, Nicolas, Moore, Marten, James, Euan K., Dietz, Karl-Josef, and Becana, Manuel. “Function of glutathione peroxidases in legume root nodules”. Journal of Experimental Botany 66.10 (2015): 2979-2990.

15 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Oxidative protein folding: state-of-the-art and current avenues of research in plants.
Meyer AJ, Riemer J, Rouhier N., New Phytol 221(3), 2019
PMID: 30230547
Sulfate is transported at significant rates through the symbiosome membrane and is crucial for nitrogenase biosynthesis.
Schneider S, Schintlmeister A, Becana M, Wagner M, Woebken D, Wienkoop S., Plant Cell Environ 42(4), 2019
PMID: 30443991
Chromium(VI) Toxicity in Legume Plants: Modulation Effects of Rhizobial Symbiosis.
Stambulska UY, Bayliak MM, Lushchak VI., Biomed Res Int 2018(), 2018
PMID: 29662899
Protein Carbonylation and Glycation in Legume Nodules.
Matamoros MA, Kim A, Peñuelas M, Ihling C, Griesser E, Hoffmann R, Fedorova M, Frolov A, Becana M., Plant Physiol 177(4), 2018
PMID: 29970413
Sulfur Transport and Metabolism in Legume Root Nodules.
Becana M, Wienkoop S, Matamoros MA., Front Plant Sci 9(), 2018
PMID: 30364181
Involvement of Glutaredoxin and Thioredoxin Systems in the Nitrogen-Fixing Symbiosis between Legumes and Rhizobia.
Alloing G, Mandon K, Boncompagni E, Montrichard F, Frendo P., Antioxidants (Basel) 7(12), 2018
PMID: 30563061
Post-translational modifications of Medicago truncatula glutathione peroxidase 1 induced by nitric oxide.
Castella C, Mirtziou I, Seassau A, Boscari A, Montrichard F, Papadopoulou K, Rouhier N, Puppo A, Brouquisse R., Nitric Oxide 68(), 2017
PMID: 28193486
Glutathione peroxidase-like enzymes cover five distinct cell compartments and membrane surfaces in Arabidopsis thaliana.
Attacha S, Solbach D, Bela K, Moseler A, Wagner S, Schwarzländer M, Aller I, Müller SJ, Meyer AJ., Plant Cell Environ 40(8), 2017
PMID: 28102911
Glutathione affects the transport activity of Rhizobium leguminosarum 3841 and is essential for efficient nodulation.
Cheng G, Karunakaran R, East AK, Munoz-Azcarate O, Poole PS., FEMS Microbiol Lett 364(8), 2017
PMID: 28333211
Identification of Salt Tolerance-related microRNAs and Their Targets in Maize (Zea mays L.) Using High-throughput Sequencing and Degradome Analysis.
Fu R, Zhang M, Zhao Y, He X, Ding C, Wang S, Feng Y, Song X, Li P, Wang B., Front Plant Sci 8(), 2017
PMID: 28603532
Reactive Oxygen Species and Nitric Oxide Control Early Steps of the Legume - Rhizobium Symbiotic Interaction.
Damiani I, Pauly N, Puppo A, Brouquisse R, Boscari A., Front Plant Sci 7(), 2016
PMID: 27092165

49 References

Daten bereitgestellt von Europe PubMed Central.

Protein S-nitrosylation: what's going on in plants?
Astier J, Kulik A, Koen E, Besson-Bard A, Bourque S, Jeandroz S, Lamotte O, Wendehenne D., Free Radic. Biol. Med. 53(5), 2012
PMID: 22750205
Proteomics gives insight into the regulatory function of chloroplast thioredoxins
Balmer Y, Koller A, del G, Manieri W, Schürmann P, Buchanan BB., 2003
Recent insights into antioxidant defenses of legume root nodules.
Becana M, Matamoros MA, Udvardi M, Dalton DA., New Phytol. 188(4), 2010
PMID: 21039567
Glutathione peroxidases
Brigelius-Flohé R, Maiorino M., 2013
ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis.
Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ., Plant J. 45(1), 2006
PMID: 16367958
Control of leghaemoglobin synthesis in snake beans.
Broughton WJ, Dilworth MJ., Biochem. J. 125(4), 1971
PMID: 5144223
Analyzing small and long RNAs in plant development using non-radioactive in situ hybridization
Bustos-Sanmamed P, Laffont C, Frugier F, Lelandais-Brière C, Crespi M., 2013
A novel approach to identify proteins modified by nitric oxide: the HIS-TAG switch method.
Camerini S, Polci ML, Restuccia U, Usuelli V, Malgaroli A, Bachi A., J. Proteome Res. 6(8), 2007
PMID: 17629318
Arabidopsis chloroplastic glutathione peroxidases play a role in cross talk between photooxidative stress and immune responses.
Chang CC, Slesak I, Jorda L, Sotnikov A, Melzer M, Miszalski Z, Mullineaux PM, Parker JE, Karpinska B, Karpinski S., Plant Physiol. 150(2), 2009
PMID: 19363092
Novel aspects of symbiotic nitrogen fixation uncovered by transcript profiling with cDNA arrays.
Colebatch G, Kloska S, Trevaskis B, Freund S, Altmann T, Udvardi MK., Mol. Plant Microbe Interact. 15(5), 2002
PMID: 12036271
Antioxidant defenses of plants and fungi
Dalton DA., 1995
Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context
Foyer CH, Noctor G., 2005
The involvement of Arabidopsis glutathione peroxidase 8 in the suppression of oxidative damage in the nucleus and cytosol.
Gaber A, Ogata T, Maruta T, Yoshimura K, Tamoi M, Shigeoka S., Plant Cell Physiol. 53(9), 2012
PMID: 22773682
Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method
Gietz RD, Woods RA., 2002
Salt and oxidative stress: similar and specific responses and their relation to salt tolerance in citrus.
Gueta-Dahan Y, Yaniv Z, Zilinskas BA, Ben-Hayyim G., Planta 203(4), 1997
PMID: 9421931

Guthrie C, Fink GR., 1991
Immunolocalization of a plant glutathione peroxidase-like protein.
Herbette S, Brunel N, Prensier G, Julien JL, Drevet JR, Roeckel-Drevet P., Planta 219(5), 2004
PMID: 15164287
Seleno-independent glutathione peroxidases. More than simple antioxidant scavengers.
Herbette S, Roeckel-Drevet P, Drevet JR., FEBS J. 274(9), 2007
PMID: 17419737
Protein S-nitrosylation: a physiological signal for neuronal nitric oxide.
Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH., Nat. Cell Biol. 3(2), 2001
PMID: 11175752
A Chinese cabbage cDNA with high sequence identity to phospholipid hydroperoxide glutathione peroxidases encodes a novel isoform of thioredoxin-dependent peroxidase.
Jung BG, Lee KO, Lee SS, Chi YH, Jang HH, Kang SS, Lee K, Lim D, Yoon SC, Yun DJ, Inoue Y, Cho MJ, Lee SY., J. Biol. Chem. 277(15), 2002
PMID: 11823460
Crystal structures of a poplar thioredoxin peroxidase that exhibits the structure of glutathione peroxidases: insights into redox-driven conformational changes.
Koh CS, Didierjean C, Navrot N, Panjikar S, Mulliert G, Rouhier N, Jacquot JP, Aubry A, Shawkataly O, Corbier C., J. Mol. Biol. 370(3), 2007
PMID: 17531267
Phospholipid hydroperoxide glutathione peroxidase.
Maiorino M, Gregolin C, Ursini F., Meth. Enzymol. 186(), 1990
PMID: 2233312
Glutathione peroxidase family - an evolutionary overview.
Margis R, Dunand C, Teixeira FK, Margis-Pinheiro M., FEBS J. 275(15), 2008
PMID: 18616466
Identification of cDNAS encoding plastid-targeted glutathione peroxidase.
Mullineaux PM, Karpinski S, Jimenez A, Cleary SP, Robinson C, Creissen GP., Plant J. 13(3), 1998
PMID: 9680987
Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation.
Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, Niwa Y, Toyooka K, Matsuoka K, Jinbo T, Kimura T., J. Biosci. Bioeng. 104(1), 2007
PMID: 17697981
Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses.
Navrot N, Collin V, Gualberto J, Gelhaye E, Hirasawa M, Rey P, Knaff DB, Issakidis E, Jacquot JP, Rouhier N., Plant Physiol. 142(4), 2006
PMID: 17071643
The effects of redox controls mediated by glutathione peroxidases on root architecture in Arabidopsis thaliana.
Passaia G, Queval G, Bai J, Margis-Pinheiro M, Foyer CH., J. Exp. Bot. 65(5), 2014
PMID: 24470466
Arabidopsis nonsymbiotic hemoglobin AHb1 modulates nitric oxide bioactivity.
Perazzolli M, Dominici P, Romero-Puertas MC, Zago E, Zeier J, Sonoda M, Lamb C, Delledonne M., Plant Cell 16(10), 2004
PMID: 15367716
Lipid peroxidation in peribacteroid membranes from French-bean nodules.
Puppo A, Herrada G, Rigaud J., Plant Physiol. 96(3), 1991
PMID: 16668260
Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process.
Puppo A, Groten K, Bastian F, Carzaniga R, Soussi M, Lucas MM, de Felipe MR, Harrison J, Vanacker H, Foyer CH., New Phytol. 165(3), 2005
PMID: 15720680
Hydrogen peroxide and nitric oxide: key regulators of the Legume-Rhizobium and mycorrhizal symbioses.
Puppo A, Pauly N, Boscari A, Mandon K, Brouquisse R., Antioxid. Redox Signal. 18(16), 2013
PMID: 23249379
The glutathione peroxidase gene family of Lotus japonicus: characterization of genomic clones, expression analyses and immunolocalization in legumes.
Ramos J, Matamoros MA, Naya L, James EK, Rouhier N, Sato S, Tabata S, Becana M., New Phytol. 181(1), 2008
PMID: 18826485
Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathways.
Rodriguez Milla MA, Maurer A, Rodriguez Huete A, Gustafson JP., Plant J. 36(5), 2003
PMID: 14617062
Cadmium-induced subcellular accumulation of O− and HO in pea leaves
Romero-Puertas MC, Rodríguez-Serrano M, Corpas FJ, Gómez M, del LA, Sandalio LM., 2004
Immunolocalization of antioxidant enzymes in high-pressure frozen root and stem nodules of Sesbania rostrata.
Rubio MC, Becana M, Kanematsu S, Ushimaru T, James EK., New Phytol. 183(2), 2009
PMID: 19594703
Plant hemoglobins may be maintained in functional form by reduced flavins in the nuclei, and confer differential tolerance to nitro-oxidative stress.
Sainz M, Perez-Rontome C, Ramos J, Mulet JM, James EK, Bhattacharjee U, Petrich JW, Becana M., Plant J. 76(5), 2013
PMID: 24118423
Leghemoglobin is nitrated in functional legume nodules in a tyrosine residue within the heme cavity by a nitrite/peroxide-dependent mechanism
Sainz M, Calvo-Begueria L, Pérez-Rontomé C, Wienkoop S, Abián J, Staudinger C, Bartesaghi S, Radi R, Becana M., 2015
Colocalization and FRET-analysis of subunits c and a of the vacuolar H+-ATPase in living plant cells.
Seidel T, Kluge C, Hanitzsch M, Ross J, Sauer M, Dietz KJ, Golldack D., J. Biotechnol. 112(1-2), 2004
PMID: 15288951
A glimpse of the mechanisms of ion homeostasis during salt stress
Serrano R, Mulet JM, Rios G., 1999
Peroxiredoxins and NADPH-dependent thioredoxin systems in the model legume Lotus japonicus.
Tovar-Mendez A, Matamoros MA, Bustos-Sanmamed P, Dietz KJ, Cejudo FJ, Rouhier N, Sato S, Tabata S, Becana M., Plant Physiol. 156(3), 2011
PMID: 21562331
Ferrous ion oxidation in presence of ferric ion indicator xylenol orange for measurement of hydroperoxides
Wolff SP., 1994

AUTHOR UNKNOWN, 0

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 25740929
PubMed | Europe PMC

Suchen in

Google Scholar