Advanced SearchSearch Tips
Thiol-Based Peroxidases and Ascorbate Peroxidases: Why Plants Rely on Multiple Peroxidase Systems in the Photosynthesizing Chloroplast?
facebook(new window)  Pirnt(new window) E-mail(new window) Excel Download
  • Journal title : Molecules and Cells
  • Volume 39, Issue 1,  2016, pp.20-25
  • Publisher : Korea Society for Molecular and Cellular Biology
  • DOI : 10.14348/molcells.2016.2324
 Title & Authors
Thiol-Based Peroxidases and Ascorbate Peroxidases: Why Plants Rely on Multiple Peroxidase Systems in the Photosynthesizing Chloroplast?
Dietz, Karl-Josef;
  PDF(new window)
Photosynthesis is a highly robust process allowing for rapid adjustment to changing environmental conditions. The efficient acclimation depends on balanced redox metabolism and control of reactive oxygen species release which triggers signaling cascades and potentially detrimental oxidation reactions. Thiol peroxidases of the peroxiredoxin and glutathione peroxidase type, and ascorbate peroxidases are the main peroxide detoxifying enzymes of the chloroplast. They use different electron donors and are linked to distinct redox networks. In addition, the peroxiredoxins serve functions in redox regulation and retrograde signaling. The complexity of plastid peroxidases is discussed in context of suborganellar localization, substrate preference, metabolic coupling, protein abundance, activity regulation, interactions, signaling functions, and the conditional requirement for high antioxidant capacity. Thus the review provides an opinion on the advantage of linking detoxification of peroxides to different enzymatic systems and implementing mechanisms for their inactivation to enforce signal propagation within and from the chloroplast.
acorbate peroxidase;chloroplast;peroxiredoxin;photosynthesis;redox sensing;
 Cited by
Overview on Peroxiredoxin,;

Molecules and Cells, 2016. vol.39. 1, pp.1-5 crossref(new window)
Peroxiredoxins and Redox Signaling in Plants, Antioxidants & Redox Signaling, 2017  crossref(new windwow)
Overview on Peroxiredoxin, Molecules and Cells, 2016, 39, 1, 1  crossref(new windwow)
Reactive Oxygen Species (ROS): Beneficial Companions of Plants’ Developmental Processes, Frontiers in Plant Science, 2016, 7  crossref(new windwow)
Tuning of Redox Regulatory Mechanisms, Reactive Oxygen Species and Redox Homeostasis under Salinity Stress, Frontiers in Plant Science, 2016, 7  crossref(new windwow)
Proteomic comparison reveals the contribution of chloroplast to salt tolerance of a wheat introgression line, Scientific Reports, 2016, 6, 1  crossref(new windwow)
Dithiol disulphide exchange in redox regulation of chloroplast enzymes in response to evolutionary and structural constraints, Plant Science, 2017, 255, 1  crossref(new windwow)
Abiotic stress: Interplay between ROS, hormones and MAPKs, Environmental and Experimental Botany, 2017, 137, 142  crossref(new windwow)
Overexpression of AhpC enhances stress tolerance and N 2 –fixation in Anabaena by upregulating stress responsive genes, Biochimica et Biophysica Acta (BBA) - General Subjects, 2016, 1860, 11, 2576  crossref(new windwow)
ROS Are Good, Trends in Plant Science, 2017, 22, 1, 11  crossref(new windwow)
An Atlas of Peroxiredoxins Created Using an Active Site Profile-Based Approach to Functionally Relevant Clustering of Proteins, PLOS Computational Biology, 2017, 13, 2, e1005284  crossref(new windwow)
GUN1, a Jack-Of-All-Trades in Chloroplast Protein Homeostasis and Signaling, Frontiers in Plant Science, 2016, 7  crossref(new windwow)
Comparative Expression Analysis of Rice and Arabidopsis Peroxiredoxin Genes Suggests Conserved or Diversified Roles Between the Two Species and Leads to the Identification of Tandemly Duplicated Rice Peroxiredoxin Genes Differentially Expressed in Seeds, Rice, 2017, 10, 1  crossref(new windwow)
Reactive oxygen species, abiotic stress and stress combination, The Plant Journal, 2017, 90, 5, 856  crossref(new windwow)
The redox-sensitive module of cyclophilin 20-3, 2-cysteine peroxiredoxin and cysteine synthase integrates sulfur metabolism and oxylipin signaling in the high light acclimation response, The Plant Journal, 2017, 91, 6, 995  crossref(new windwow)
Plant growth-promoting endophyte Sphingomonas sp. LK11 alleviates salinity stress in Solanum pimpinellifolium, Environmental and Experimental Botany, 2017, 133, 58  crossref(new windwow)
Redox and Reactive Oxygen Species Network in Acclimation for Salinity Tolerance in Sugar Beet, Journal of Experimental Botany, 2017, 68, 5, 1283  crossref(new windwow)
Allahverdiyeva, Y., Suorsa, M., Tikkanen, M., and Aro, E.M. (2015). Photoprotection of photosystems in fluctuating light intensities. J. Exp. Bot. 66, 2427-2436. crossref(new window)

Asada, K. (1999). The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 601-639. crossref(new window)

Awad, J., Stotz, H.U., Fekete, A., Krischke, M., Engert, C., Havaux, M., Berger, S., and Mueller, M.J. (2015). 2-cysteine peroxiredoxins and thylakoid ascorbate peroxidase create a water-water cycle that is essential to protect the photosynthetic apparatus under high light stress conditions. Plant Physiol. 167, 1592-1603. crossref(new window)

Badger, M.R., von Caemmerer, S., Ruuska, S., and Nakano, H. (2000). Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and Rubisco oxygenase. Philos. Trans. R. Soc. B: Biol. Sci. 355, 1433-1446. crossref(new window)

Baier, M., and Dietz, K.J. (1999). Protective function of chloroplast 2-Cys peroxiredoxin in photosynthesis: Evidence from transgenic Arabidopsis thaliana. Plant Physiol. 119, 1407-1414. crossref(new window)

Baier, M., Noctor, G., Foyer, C.H., and Dietz, K.J. (2000). Antisense suppression of 2-Cys peroxiredoxin in Arabidopsis thaliana specifically enhances the activities and expression of enzymes associated with ascorbate metabolism, but not glutathione metabolism. Plant Physiol. 124, 823-832. crossref(new window)

Bertoldi, M. (2016). Human peroxiredoxins 1 and 2 and their interacting protein partners; through structure toward functions of biological complexes. Protein Pept. Lett. [in press].

Broin, M., Cuine, S., Eymery, F., and Rey, P. (2002). The plastidic 2-cysteine peroxiredoxin is a target for a thioredoxin involved in the protection of the photosynthetic apparatus against oxidative damage. Plant Cell 14, 1417-1432. crossref(new window)

Caporaletti, D., D'Alessio, A.C., Rodriguez-Suarez, R.J., Senn, A.M., Duek, P.D., and Wolosiuk, R.A. (2007). Non-reductive modulation of chloroplast fructose-1,6-bisphosphatase by 2-Cys peroxiredoxin. Biochem. Biophys. Res. Commun. 355, 722-727. crossref(new window)

Caverzan, A., Bonifacio, A., Carvalho, F.E., Andrade, C.M., Passaia, G., Schunemann, M., Maraschin Fdos, S., Martins, M.O., Teixeira, F.K., Rauber, R., et al. (2014). The knockdown of chloroplastic ascorbate peroxidases reveals its regulatory role in the photosynthesis and protection under photo-oxidative stress in rice. Plant Sci. 214, 74-87. crossref(new window)

Cerveau, D., Ouahrani, D., Marok, M.A., Blanchard, L., and Rey, P. (2016). Physiological relevance of plant 2-Cys peroxiredoxin overoxidation level and oligomerization status. Plant Cell Environ. [in press].

Chae, H.Z., Oubrahim, H., Park, J.W., Rhee, S.G., and Chock, P.B. (2012). Protein glutathionylation in the regulation of peroxiredoxins: a family of thiol-specific peroxidases that function as antioxidants, molecular chaperones, and signal modulators. Antioxid. Redox. Signal. 16, 506-523. crossref(new window)

Chang, C.C., Slesak, I., Jorda, L., Sotnikov, A., Melzer, M., Miszalski, Z., Mullineaux, P.M., Parker, J.E., Karpinska, B., and Karpinski, S. (2009). Arabidopsis chloroplastic glutathione peroxidases play a role in cross talk between photooxidative stress and immune responses. Plant Physiol. 150, 670-683. crossref(new window)

Collin, V., Issakidis-Bourguet, E., Marchand, C., Hirasawa, M., Lancelin, J.M., Knaff, D.B., and Miginiac-Maslow, M. (2003). The Arabidopsis plastidial thioredoxins: new functions and new insights into specificity. J. Biol. Chem. 278, 23747-23752. crossref(new window)

Couturier, J., Stroher, E., Albetel, A.N., Roret, T., Muthuramalingam, M., Tarrago, L., Seidel, T., Tsan, P., Jacquot, J.P., Johnson, M.K. et al. (2011). Arabidopsis chloroplastic glutaredoxin C5 as a model to explore molecular determinants for iron-sulfur cluster binding into glutaredoxins. J. Biol. Chem. 286, 27515-27527. crossref(new window)

Dalal, A., Vishwakarma, A., Singh, N.K., Gudla, T., Bhattacharyya, M.K., Padmasree, K., Viehhauser, A., Dietz, K.J., and Kirti, P.B. (2014). Attenuation of hydrogen peroxide-mediated oxidative stress by Brassica juncea annexin-3 counteracts thiol-specific antioxidant (TSA1) deficiency in Saccharomyces cerevisiae. FEBS Lett. 588, 584-593. crossref(new window)

Dangoor, I., Peled-Zehavi, H., Levitan, A., Pasand, O., and Danon, A. (2009). A small family of chloroplast atypical thioredoxins. Plant Physiol. 149, 1240-1250. crossref(new window)

Dietz, K.J., Jacob, S., Oelze, M.L., Laxa, M., Tognetti, V., de Miranda, S.M., Baier, M., and Finkemeier, I. (2006). The function of peroxiredoxins in plant organelle redox metabolism. J. Exp. Bot. 57, 1697-1709. crossref(new window)

Dietz, K.J., and Hell, R. (2015). Thiol switches in redox regulation of chloroplasts: balancing redox state, metabolism and oxidative stress. Biol Chem. 396, 483-494.

Dixon, D.P., Hawkins, T., Hussey, P.J., and Edwards, R. (2009). Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily. J. Exp. Bot. 60, 1207-1218. crossref(new window)

Eshdat, Y., Holland, D., Faltin, Z., and BenHayyim, G. (1997). Plant glutathione peroxidases. Physiol. Plant 100, 234-240. crossref(new window)

Farmer, E.E., and Mueller, M.J. (2013). ROS-mediated lipid peroxidation and RES-activated signaling. Annu. Rev. Plant Biol. 64, 429-450. crossref(new window)

Ferro, M., Brugiere, S., Salvi, D., Seigneurin-Berny, D., Court, M., Moyet, L., Ramus, C., Miras, S., Mellal, M., Le Gall, S., et al. (2010). AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol. Cell Proteomics 9, 1063-1084. crossref(new window)

Flohe, L. (2015). The impact of thiol peroxidases on redox regulation. Free Radic. Res. 14, 1-17.

Heyno, E., Gross, C.M., Laureau, C., Culcasi, M., Pietri, S., and Krieger-Liszkay, A. (2009). Plastid alternative oxidase (PTOX) promotes oxidative stress when overexpressed in tobacco. J. Biol. Chem. 284, 31174-31180. crossref(new window)

Jang, H.H., Lee, K.O., Chi, Y.H., Jung, B.G., Park, S.K., Park, J.H., Lee, J.R., Lee, S.S., Moon, J.C., Yun, J.W., et al. (2004). Two enzymes in one; two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell 117, 625-635. crossref(new window)

Kangasjarvi, S., Lepisto, A., Hannikainen, K., Piippo, M., Luomala, E.M., Aro, E.M., and Rintamaki, E. (2008). Diverse roles for chloroplast stromal and thylakoid-bound ascorbate peroxidases in plant stress responses. Biochem. J. 412, 275-285. crossref(new window)

Kim, K., Kim, I.H., Lee, K.Y., Rhee, S.G., and Stadtman, E.R. (1988). The isolation and purification of a specific "protector" protein which inhibits enzyme inactivation by a thiol/Fe(III)/O2 mixedfunction oxidation system. J. Biol. Chem. 263, 4704-4711.

Kitajima, S. (2008). Hydrogen peroxide-mediated inactivation of two chloroplastic peroxidases, ascorbate peroxidase and 2-cys peroxiredoxin. Photochem. Photobiol. 84, 1404-1409. crossref(new window)

Konig, J., Lotte, K., Plessow, R., Brockhinke, A., Baier, M., and Dietz, K.J. (2003). Reaction mechanism of the 2-Cys peroxiredoxin:Role of the C-terminus and the quarternary structure. J. Biol. Chem. 278, 24409-24420. crossref(new window)

Konig, J., Muthuramalingam, M., and Dietz, K.J. (2012). Mechanisms and dynamics in the thiol/disulfide redox regulatory network:transmitters, sensors and targets. Curr. Opin. Plant Biol. 15, 261-268. crossref(new window)

Konig, J., Galliardt, H., Jutte, P., Schaper, S., Dittmann, L., and Dietz, K.J. (2013). The conformational bases for the two functionalities of 2-Cys peroxiredoxins as peroxidase and chaperone. J. Exp. Bot. 64, 3483-3497. crossref(new window)

Laisk, A., Eichelmann, H., Oja, V., Rasulov, B. ,and Ramma, H. (2006). Photosystem II cycle and alternative electron flow in leaves. Plant Cell Physiol. 47, 972-983. crossref(new window)

Lamkemeyer, P., Laxa, M., Collin, V., Li, W., Finkemeier, I., Schottler, M.A., Holtkamp, V., Tognetti, V.B., Issakidis-Bourguet, E., Kandlbinder, A., et al. (2006). Peroxiredoxin Q of Arabidopsis thaliana is attached to the thylakoids and functions in context of photosynthesis. Plant J. 45, 968-981. crossref(new window)

Lee, E.M., Lee, S.S., Tripathi, B.N., Jung, H.S., Cao, G.P., Lee, Y., Singh, S., Hong, S.H., Lee, K.W., Lee, S.Y., et al. (2015). Sitedirected mutagenesis substituting cysteine for serine in 2-Cys peroxiredoxin (2-Cys Prx A) of Arabidopsis thaliana effectively improves its peroxidase and chaperone functions. Ann. Bot. 116, 713-725. crossref(new window)

Liebthal, M., Struve, M., Li, X., Hertle, Y., Maynard, D., Hellweg, T., Viehhauser, A., and Dietz, K.J. (2016). Redox-dependent conformational dynamics of decameric 2-cysteine peroxiredoxin and its interaction with cyclophilin Cyp20-3. Plant Cell Physiol. resubmitted, provisional acceptance.

Liu, X.P., Liu, X.Y., Zhang, J., Xia, Z.L., Liu, X., Qin, H.J., and Wang, D.W. (2006). Molecular and functional characterization of sulfiredoxin homologs from higher plants. Cell Res. 16, 287-296. crossref(new window)

Liu, K.L., Shen, L., Wang, J.Q., and Sheng, J.P. (2008). Rapid inactivation of chloroplastic ascorbate peroxidase is responsible for oxidative modification to Rubisco in tomato (Lycopersicon esculentum) under cadmium stress. J. Integr. Plant Biol. 50, 415-426. crossref(new window)

Matamoros, M.A., Saiz, A., Penuelas, 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. J. Exp. Bot. 66, 2979-2990. crossref(new window)

Mittler, R., Vanderauwera, S., Gollery, M., and Van Breusegem, F. (2004). Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490-498. crossref(new window)

Miyake, C., and Asada, K. (1996) Inactivation mechanism of ascorbate peroxidase at low concentrations of ascorbate; hydrogen peroxide decomposes compound I of ascorbate peroxidase. Plant Cell Physiol. 37, 423-430. crossref(new window)

Muthuramalingam, M., Seidel, T., Laxa, M., Nunes de Miranda, S., Gartner, F., Stroher, E., Kandlbinder, A., and Dietz, K.J. (2009). Multiple redox and non-redox interactions define 2-Cys peroxiredoxin as a regulatory hub in the chloroplast. Mol. Plant 2, 1273-1288. crossref(new window)

Nakano, Y., and Asada, K. (1987). Purification of ascorbate peroxidase in spinach chloroplasts; its inactivation in ascorbatedepleted medium and reactivation by monodehydroascorbate radical. Plant Cell Physiol. 28, 131-140.

Navrot, N., Collin, V., Gualberto, J., Gelhaye, E., Hirasawa, M., Rey, P., Knaff, D.B., Issakidis, E., Jacquot, J.P., and Rouhier, N. (2006). Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiol. 142, 1364-1379. crossref(new window)

Naranjo, B., Mignee, C., Krieger-Liszkay, A., Hornero-Mendez, D., Gallardo-Guerrero, L., Cejudo, F.J., and Lindahl, M. (2016). The chloroplast NADPH thioredoxin reductase C, NTRC, controls non-photochemical quenching of light energy and photosynthetic electron transport in Arabidopsis. Plant Cell Environ. [in press].

Obayashi, T., Hayashi, S., Saeki, M., Ohta, H., and Kinoshita, K. (2009). ATTED-II provides coexpressed gene networks for Arabidopsis. Nucleic Acids Res. 37, D987-91. crossref(new window)

Pena-Ahumada, A., Kahmann, U., Dietz, K.J., and Baier, M. (2006). Antioxidant defence in seedling development of Arabidopsis thaliana. Photosynthesis Res. 89, 99-112. crossref(new window)

Petersson, U.A., Kieselbach, T., Garcia-Cerdan, J.G., and Schroder, W.P. (2006). The Prx Q protein of Arabidopsis thaliana is a member of the luminal chloroplast proteome. FEBS Lett. 580, 6055-6061. crossref(new window)

Polle, A. (2001). Dissecting the superoxide dismutase-ascorbateglutathione-pathway in chloroplasts by metabolic modeling. Computer simulations as a step towards flux analysis. Plant Physiol. 126, 445-462. crossref(new window)

Pulido, P., Spinola, M.C., Kirchsteiger, K., Guinea, M., Pascual, M.B., Sahrawy, M., Sandalio, L.M., Diet,z .K.J, Gonzalez, M., and Cejudo, F.J. (2010). Functional analysis of the pathways for 2-Cys peroxiredoxin reduction in Arabidopsis thaliana chloroplasts. J. Exp. Bot. 61, 4043-4054. crossref(new window)

Romero-Puertas, M.C., Laxa, M., Matte, A., Zaninotto, F., Finkemeier, I., Jones, A.M., Perazzolli, M., Vandelle, E., Dietz, K.J., and Delledonne, M. (2007). S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell 19, 4120-4130. crossref(new window)

Ruuska, S.A., Badger, M.R., Andrews, T.J., and von Caemmerer, S. (2000). Photosynthetic electron sinks in transgenic tobacco with reduced amounts of Rubisco: little evidence for significant Mehler reaction. J. Exp. Bot. 51, 357-368. crossref(new window)

Seo, J.H., Lim, J.C., Lee, D.Y., Kim, K.S., Piszczek, G., Nam, H.W., Kim, Y.S., Ahn, T., Yun, C.H., Kim, K., et al. (2009). Novel protective mechanism against irreversible hyperoxidation of peroxiredoxin: N-alpha-terminal acetylation of human peroxiredoxin II. J. Biol. Chem. 284, 13455-13465. crossref(new window)

Shirao, M., Kuroki, S., Kaneko, K., Kinjo, Y., Tsuyama, M., Forster, B., Takahashi, S., and Badger, M.R. (2013). Gymnosperms have increased capacity for electron leakage to oxygen (Mehler and PTOX reactions) in photosynthesis compared with angiosperms. Plant Cell Physiol. 54, 1152-1163. crossref(new window)

Zhai, C.Z., Zhao, L., Yin, L.J., Chen, M., Wang, Q.Y., Li, L.C., Xu, Z.S., and You-Zhi Ma, Y.Z. (2013). Two wheat glutathione peroxidase genes whose products are located in chloroplasts improve salt and $H_2O_2$ tolerances in Arabidopsis. PLoS One 8, e73989. crossref(new window)