The hydrogen peroxide-sensitive proteome of the chloroplast in vitro and in vivo

Muthuramalingam M, Matros A, Scheibe R, Mock H-P, Dietz K-J (2013)
Frontiers in Plant Science 4: 54-1-54-14.

Download
OA
Journal Article | Published | English
Author
; ; ; ;
Abstract
Hydrogen peroxide (H2O2) evolves during cellular metabolism and accumulates under various stresses causing serious redox imbalances. Many proteomics studies aiming to identify proteins sensitive to H2O2 used concentrations that were above the physiological range. Here the chloroplast proteins were subjected to partial oxidation by exogenous addition of H2O2 equivalent to 10% of available protein thiols which allowed for the identification of the primary targets of oxidation. The chosen redox proteomic approach employed differential labeling of non-oxidized and oxidized thiols using sequential alkylation with N-ethylmaleimide and biotin maleimide. The in vitro identified proteins are involved in carbohydrate metabolism, photosynthesis, redox homeostasis, and nitrogen assimilation. By using methyl viologen that induces oxidative stress in vivo, mostly the same primary targets of oxidation were identified and several oxidation sites were annotated. Ribulose-1,5-bisphosphate (RubisCO) was a primary oxidation target. Due to its high abundance, RubisCO is suggested to act as a chloroplast redox buffer to maintain a suitable redox state, even in the presence of increased reactive oxygen species release. 2-cysteine peroxiredoxins (2-Cys Prx) undergo redox-dependent modifications and play important roles in antioxidant defense and signaling. The identification of 2-Cys Prx was expected based on its high affinity to H2O2 and is considered as a proof of concept for the approach. Targets of Trx, such as phosphoribulokinase, glyceraldehyde-3-phosphate dehydrogenase, transketolase, and sedoheptulose-1,7-bisphosphatase have at least one regulatory disulfide bridge which supports the conclusion that the identified proteins undergo reversible thiol oxidation. In conclusion, the presented approach enabled the identification of early targets of H2O2 oxidation within the cellular proteome under physiological experimental conditions.
Publishing Year
ISSN
eISSN
PUB-ID

Cite this

Muthuramalingam M, Matros A, Scheibe R, Mock H-P, Dietz K-J. The hydrogen peroxide-sensitive proteome of the chloroplast in vitro and in vivo. Frontiers in Plant Science. 2013;4:54-1-54-14.
Muthuramalingam, M., Matros, A., Scheibe, R., Mock, H. - P., & Dietz, K. - J. (2013). The hydrogen peroxide-sensitive proteome of the chloroplast in vitro and in vivo. Frontiers in Plant Science, 4, 54-1-54-14.
Muthuramalingam, M., Matros, A., Scheibe, R., Mock, H. - P., and Dietz, K. - J. (2013). The hydrogen peroxide-sensitive proteome of the chloroplast in vitro and in vivo. Frontiers in Plant Science 4, 54-1-54-14.
Muthuramalingam, M., et al., 2013. The hydrogen peroxide-sensitive proteome of the chloroplast in vitro and in vivo. Frontiers in Plant Science, 4, p 54-1-54-14.
M. Muthuramalingam, et al., “The hydrogen peroxide-sensitive proteome of the chloroplast in vitro and in vivo”, Frontiers in Plant Science, vol. 4, 2013, pp. 54-1-54-14.
Muthuramalingam, M., Matros, A., Scheibe, R., Mock, H.-P., Dietz, K.-J.: The hydrogen peroxide-sensitive proteome of the chloroplast in vitro and in vivo. Frontiers in Plant Science. 4, 54-1-54-14 (2013).
Muthuramalingam, Meenakumari, Matros, Andrea, Scheibe, Renate, Mock, Hans-Peter, and Dietz, Karl-Josef. “The hydrogen peroxide-sensitive proteome of the chloroplast in vitro and in vivo”. Frontiers in Plant Science 4 (2013): 54-1-54-14.
Main File(s)
Access Level
OA Open Access
Last Uploaded
2013-04-16 11:42:07

This data publication is cited in the following publications:
This publication cites the following data publications:

19 Citations in Europe PMC

Data provided by Europe PubMed Central.

Protein Phosphorylation and Redox Modification in Stomatal Guard Cells.
Balmant KM, Zhang T, Chen S., Front Physiol 7(), 2016
PMID: 26903877
Redox proteomics of tomato in response to Pseudomonas syringae infection.
Balmant KM, Parker J, Yoo MJ, Zhu N, Dufresne C, Chen S., 2015
PMID: 26504582
Potato Annexin STANN1 Promotes Drought Tolerance and Mitigates Light Stress in Transgenic Solanum tuberosum L. Plants.
Szalonek M, Sierpien B, Rymaszewski W, Gieczewska K, Garstka M, Lichocka M, Sass L, Paul K, Vass I, Vankova R, Dobrev P, Szczesny P, Marczewski W, Krusiewicz D, Strzelczyk-Zyta D, Hennig J, Konopka-Postupolska D., PLoS ONE 10(7), 2015
PMID: 26172952
Cysteines under ROS attack in plants: a proteomics view.
Akter S, Huang J, Waszczak C, Jacques S, Gevaert K, Van Breusegem F, Messens J., J. Exp. Bot. 66(10), 2015
PMID: 25750420
DYn-2 Based Identification of Arabidopsis Sulfenomes.
Akter S, Huang J, Bodra N, De Smet B, Wahni K, Rombaut D, Pauwels J, Gevaert K, Carroll K, Van Breusegem F, Messens J., Mol. Cell Proteomics 14(5), 2015
PMID: 25693797
Direct determination of the redox status of cysteine residues in proteins in vivo.
Hara S, Tatenaka Y, Ohuchi Y, Hisabori T., Biochem. Biophys. Res. Commun. 456(1), 2015
PMID: 25436431
Expression of an evolved engineered variant of a bacterial glycine oxidase leads to glyphosate resistance in alfalfa.
Nicolia A, Ferradini N, Molla G, Biagetti E, Pollegioni L, Veronesi F, Rosellini D., J. Biotechnol. 184(), 2014
PMID: 24905148
Insight into protein S-nitrosylation in Chlamydomonas reinhardtii.
Morisse S, Zaffagnini M, Gao XH, Lemaire SD, Marchand CH., Antioxid. Redox Signal. 21(9), 2014
PMID: 24328795
CP12-mediated protection of Calvin-Benson cycle enzymes from oxidative stress.
Marri L, Thieulin-Pardo G, Lebrun R, Puppo R, Zaffagnini M, Trost P, Gontero B, Sparla F., Biochimie 97(), 2014
PMID: 24211189
Redox control of plant growth and development
Kocsy G, Tari I, Vankova R, Zechmann B, Gulyas Z, Poor P, Galiba G., Plant Sci. 211(), 2013
PMID: IND500688870
Redox regulation of the Calvin-Benson cycle: something old, something new.
Michelet L, Zaffagnini M, Morisse S, Sparla F, Perez-Perez ME, Francia F, Danon A, Marchand CH, Fermani S, Trost P, Lemaire SD., Front Plant Sci 4(), 2013
PMID: 24324475
Redox control of plant growth and development.
Kocsy G, Tari I, Vankova R, Zechmann B, Gulyas Z, Poor P, Galiba G., Plant Sci. 211(), 2013
PMID: 23987814

63 References

Data provided by Europe PubMed Central.

Dissecting the superoxide dismutase-ascorbate-glutathione-pathway in chloroplasts by metabolic modeling.
Polle A.., 2001
Identification of plant glutaredoxin targets.
Rouhier N, Villarejo A, Srivastava M, Gelhaye E, Keech O, Droux M, Finkemeier I, Samuelsson G, Dietz KJ, Jacquot JP, Wingsle G., Antioxid. Redox Signal. 7(7-8), 2005
PMID: 15998247
Co-existence of two regulatory NADP-glyceraldehyde 3-P dehydrogenase complexes in higher plant chloroplasts.
Scheibe R, Wedel N, Vetter S, Emmerlich V, Sauermann SM., Eur. J. Biochem. 269(22), 2002
PMID: 12423361
Isotope-coded affinity tag (ICAT) approach to redox proteomics: identification and quantitation of oxidant-sensitive cysteine thiols in complex protein mixtures.
Sethuraman M, McComb ME, Huang H, Huang S, Heibeck T, Costello CE, Cohen RA., J. Proteome Res. 3(6), 2004
PMID: 15595732
Proteomic signatures uncover hydrogen peroxide and nitric oxide cross-talk signaling network in citrus plants.
Tanou G, Job C, Belghazi M, Molassiotis A, Diamantidis G, Job D., J. Proteome Res. 9(11), 2010
PMID: 20825250
Glutathionylation in the photosynthetic model organism Chlamydomonas reinhardtii: a proteomic survey.
Zaffagnini M., Bedhomme M., Groni H., Marchand C., Puppo C., Gontero B.., 2012

Export

0 Marked Publications

Open Data PUB

Web of Science

View record in Web of Science®

Sources

PMID: 23516120
PubMed | Europe PMC

Search this title in

Google Scholar