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Acta Physiologiae Plantarum

, 39:57 | Cite as

Immunological evidence for the presence of peroxiredoxin in pea leaf peroxisomes and response to oxidative stress conditions

  • Francisco J. CorpasEmail author
  • José R. Pedrajas
  • José M. Palma
  • Raquel Valderrama
  • Marta Rodríguez-Ruiz
  • Mounira Chaki
  • Luis A. del Río
  • Juan B. Barroso
Original Article

Abstract

Peroxiredoxins (Prxs) constitute a group of thiol-specific antioxidant enzymes which are present in bacteria, yeasts, and in plant and animal cells. Although Prxs are mainly localized in the cytosol, they are also present in mitochondria, chloroplasts, and nuclei, but there is no evidence of the existence of Prxs in plant peroxisomes. Using soluble fractions (matrices) of peroxisomes purified from leaves of pea (Pisum sativum L.) plants, the immunological analysis with affinity-purified IgG against yeast Prx1 revealed the presence of an immunoreactive band of about 50 kDa. The apparent molecular mass of the peroxisomal Prx was not sensitive to oxidizing and reducing conditions what could be a mechanism of protection against the oxidative environment existing in peroxisomes. Postembedment, EM immunocytochemical analysis with affinity-purified IgG against yeast Prx1 antibodies, confirmed that this protein was present in the peroxisomal matrix, mitochondria, and chloroplasts. In pea plants grown under oxidative stress conditions, the protein level of peroxisomal Prx was differentially modulated, being slightly induced by growth of plants with 50 µM CdCl2, but being significantly reduced by treatment with the herbicide 2,4-dichlorophenoxyacetic acid (2,4-D). The presence in the matrix of peroxisomes of a protein immunorelated to Prx of about 50 kDa, which is in the range of molecular mass of the dimeric form of other Prxs, opens new questions on the molecular properties of Prxs, but also on their function in the metabolism of reactive oxygen and nitrogen species (ROS/RNS) in these plant cell organelles, where they could be involved in the regulation of hydrogen peroxide and/or peroxynitrite.

Keywords

Peroxiredoxin Peroxisomes Pea leaves Pisum sativum Oxidative stress Nitrosative stress 

Notes

Acknowledgements

This work was supported by ERDF-cofinanced grants from the Ministry of Science and Innovation (BIO2012-33904) and Junta de Andalucía (research groups CVI 192 and CVI 286). Present research for FJC and JMP is supported by the ERDF-cofinanced grant AGL2015-65104-P and for JBB the BIO2015-66390-P grant both from the Ministry of Economy and Competitiveness (MINECO), Spain. The electron microscopy assays were carried out at the Centre of Scientific Instrumentation of the University of Granada. The valuable technical assistance of Mr. Carmelo Ruíz-Torres is acknowledged.

Supplementary material

11738_2017_2356_MOESM1_ESM.pptx (57 kb)
Supplementary material 1 (PPTX 56 kb)

References

  1. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126CrossRefPubMedGoogle Scholar
  2. Baker A, Graham I (2002) Plant peroxisomes. Biochemistry, cell biology and biotechnological applications. Kluwer Academic, DordrechtGoogle Scholar
  3. Barranco-Medina S, López-Jaramillo FJ, Bernier-Villamor L, Sevilla F, Lazaro JJ (2006) Cloning, overexpression, purification and preliminary crystallographic studies of a mitochondrial type II peroxiredoxin from Pisum sativum. Acta Crystallogr Sect F Struct Biol Cryst Commun 62:695–698CrossRefPubMedPubMedCentralGoogle Scholar
  4. Barranco-Medina S, Krell T, Finkemeier I, Sevilla F, Lázaro JJ, Dietz KJ (2007) Biochemical and molecular characterization of the mitochondrial peroxiredoxin PsPrxII F from Pisum sativum. Plant Physiol Biochem 45:729–739CrossRefPubMedGoogle Scholar
  5. Barranco-Medina S, Lázaro JJ, Dietz KJ (2009) The oligomeric conformation of peroxiredoxins links redox state to function. FEBS Lett 583:1809–1816CrossRefPubMedGoogle Scholar
  6. Barroso JB, Corpas FJ, Carreras A, Sandalio LM, Valderrama R, Palma JM, Lupiáñez JA, del Río LA (1999) Localization of nitric oxide synthase in plant peroxisomes. J Biol Chem 274:36729–36733CrossRefPubMedGoogle Scholar
  7. Bernier-Villamor L, Navarro E, Sevilla F, Lázaro JJ (2004) Cloning and characterization of a 2-Cys peroxiredoxin from Pisum sativum. J Exp Bot 55:2191–2199CrossRefPubMedGoogle Scholar
  8. Bhatt I, Tripathi BN (2011) Plant peroxiredoxins: catalytic mechanisms, functional significance and future perspectives. Biotechnol Adv 29:850–859CrossRefPubMedGoogle Scholar
  9. Bryk R, Griffin P, Nathan C (2000) Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407:211–215CrossRefPubMedGoogle Scholar
  10. Bunkelmann JR, Trelease RN (1996) Ascorbate peroxidase. A prominent membrane protein in oilseed glyoxysomes. Plant Physiol 110:589–598CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cerveau D, Ouahrani D, Marok MA, Blanchard L, Rey P (2016) Physiological relevance of plant 2-Cys peroxiredoxin overoxidation level and oligomerization status. Plant Cell Environ 39:103–119CrossRefPubMedGoogle Scholar
  12. Chaki M, Álvarez de Morales P, Ruiz C, Begara-Morales JC, Barroso JB, Corpas FJ, Palma JM (2015) Ripening of pepper (Capsicum annuum) fruit is characterized by an enhancement of protein tyrosine nitration. Ann Bot 116:637–647CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chevenet F, Brun C, Banuls AL, Jacq B, Chisten R (2006) TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinform 7:439CrossRefGoogle Scholar
  14. Corpas FJ (2015) What is the role of hydrogen peroxide in plant peroxisomes? Plant Biol (Stuttg) 17:1099–1103CrossRefGoogle Scholar
  15. Corpas FJ, Barroso JB (2014) Peroxynitrite (ONOO) is endogenously produced in Arabidopsis peroxisomes and is overproduced under cadmium stress. Ann Bot 113:87–96CrossRefPubMedGoogle Scholar
  16. Corpas FJ, Barroso JB (2016) Lead-induced stress, which triggers the production of nitric oxide (NO) and superoxide anion (O2·−) in Arabidopsis peroxisomes, affects catalase activity. Nitric Oxide Biol Chem. doi: 10.1016/j.niox.2016.12.010 Google Scholar
  17. Corpas FJ, Trelease RN (1998) Differential expression of ascorbate peroxidase and a putative molecular chaperone in the boundary membrane of differentiating cucumber seedling peroxisomes. J Plant Physiol 153:332–338CrossRefGoogle Scholar
  18. Corpas FJ, Palma JM, del Río LA (1993) Evidence for the presence of proteolytic activity in peroxisomes. Eur J Cell Biol 61:81–85PubMedGoogle Scholar
  19. Corpas FJ, Bunkelmann J, Trelease RN (1994) Identification and immunochemical characterization of a family of peroxisome membrane proteins (PMPs) in oilseed glyoxysomes. Eur J Cell Biol 65:280–290PubMedGoogle Scholar
  20. Corpas FJ, de la Colina C, Sánchez-Rasero F, del Río LA (1997) A role for leaf peroxisomes in the catabolism of purines. J Plant Physiol 151:246–250CrossRefGoogle Scholar
  21. Corpas FJ, Sandalio LM, del Río LA, Trelease RN (1998) Copper–zinc superoxide dismutase is a constituent enzyme of the matrix of peroxisomes in the cotyledons of oilseed plants. New Phytol 138:307–314CrossRefGoogle Scholar
  22. Corpas FJ, Barroso JB, Sandalio LM, Palma JM, Lupiáñez JA, del Río LA (1999) Peroxisomal NADP-dependent isocitrate dehydrogenase. characterization and activity regulation during natural senescence. Plant Physiol 121:921–928CrossRefPubMedPubMedCentralGoogle Scholar
  23. Corpas FJ, Palma JM, Sandalio LM, Valderrama R, Barroso JB, del Río LA (2008) Peroxisomal xanthine oxidoreductase: characterization of the enzyme from pea (Pisum sativum L.) leaves. J Plant Physiol 165:1319–1330CrossRefPubMedGoogle Scholar
  24. Corpas FJ, Barroso JB, Palma JM, del Río LA (2013a) Peroxisomes as cell generators of reactive nitrogen species (RNS) signal molecules. Subcell Biochem 69:283–298CrossRefPubMedGoogle Scholar
  25. Corpas FJ, Leterrier M, Begara-Morales JC, Valderrama R, Chaki M, Jaramillo López-, Luque F, Palma JM, Padilla MN, Sánchez-Calvo B, Mata-Pérez C, Barroso JB (2013b) Inhibition of peroxisomal hydroxypyruvate reductase (HPR1) by tyrosine nitration. Biochim Biophys Acta 1830:4981–4989CrossRefPubMedGoogle Scholar
  26. Corpas FJ, Barroso JB, Palma JM, Rodriguez-Ruiz M (2017) Plant peroxisomes: a nitro-oxidative cocktail. Redox Biol. 11:535–542. doi:  10.1016/j.redox.2016.12.033 CrossRefPubMedPubMedCentralGoogle Scholar
  27. del Río LA (2011) Peroxisomes as a cellular source of reactive nitrogen species signal molecules. Arch Biochem Biophys 506:1–11CrossRefPubMedGoogle Scholar
  28. del Río LA (ed) (2013) Peroxisomes and their key role in cellular signaling and metabolism. Springer, DordrechtGoogle Scholar
  29. del Río LA, López-Huertas E (2016) ROS generation in peroxisomes and its role in cell signaling. Plant Cell Physiol 57:1364–1376PubMedGoogle Scholar
  30. del Río LA, Corpas FJ, Sandalio LM, Palma JM, Gómez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53:1255–1272CrossRefPubMedGoogle Scholar
  31. del Río LA, Sandalio LM, Altomare DA, Zilinskas BA (2003) Mitochondrial and peroxisomal manganese superoxide dismutase: differential expression during leaf senescence. J Exp Bot 54:923–933CrossRefPubMedGoogle Scholar
  32. del Río LA, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141:330–335CrossRefPubMedPubMedCentralGoogle Scholar
  33. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008). Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36(web server issue):W465–W469Google Scholar
  34. Dietz K-J (2003) Plant peroxiredoxins. Annu Rev Plant Biol 54:93–107CrossRefPubMedGoogle Scholar
  35. Dietz KJ (2011) Peroxiredoxins in plants and cyanobacteria. Antioxid Redox Signal 15:1129–1159CrossRefPubMedPubMedCentralGoogle Scholar
  36. Dietz K-J, Jacob S, Oelze M-L, Laxa M, Tognetti V, Nunes de Miranda SM, Baier M, Finkemeier I (2006) The function of peroxiredoxins in plant organelle redox metabolism. J Exp Bot 57:1697–1709CrossRefPubMedGoogle Scholar
  37. Distefano S, Palma JM, Gómez M, del Río LA (1997) Characterization of endoproteases from plant peroxisomes. Biochem J 327:399–405CrossRefPubMedPubMedCentralGoogle Scholar
  38. Fahimi HD, Reich D, Völkl A, Baumgart E (1996) Contributions of the immunogold technique to investigation of the biology of peroxisomes. Histochem Cell Biol 106:105–114CrossRefPubMedGoogle Scholar
  39. Finkemeier I, Goodman M, Lamkemeyer P, Kandlbinder A, Sweetlove LJ, Dietz K-J (2005) The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress. J Biol Chem 280:12168–12180CrossRefPubMedGoogle Scholar
  40. Groten K, Dutilleul C, van Heerden PD, Vanacker H, Bernard S, Finkemeier I, Dietz K-J, Foyer CH (2006) Redox regulation of peroxiredoxin and proteinases by ascorbate and thiols during pea root nodule senescence. FEBS Lett 580:1269–1276CrossRefPubMedGoogle Scholar
  41. Harboe HMG, Ingild A (1983) Immunization, isolation of immunoglobulins and antibody titer determination. In: Axelsen NH (ed) Handbook of immunoprecipitation-in-gel techniques. Blackwell, Oxford, pp 345–351Google Scholar
  42. Haslekas C, Grini PE, Nordgard SH, Thorstensen T, Viken MK, Nygaard V, Aalen RB (2003) ABI3 mediates expression of the peroxiredoxin antioxidant AtPER1 gene and induction by oxidative stress. Plant Mol Biol 53:313–326CrossRefPubMedGoogle Scholar
  43. Horiguchi H, Yurimoto H, Kato N, Sakai Y (2001) Antioxidant system within yeast peroxisome. Biochemical and physiological characterization of CbPmp20 in the methylotrophic yeast Candida boidinii. J Biol Chem 276:14279–14288PubMedGoogle Scholar
  44. Horling F, König J, Dietz K-J (2002) Type II peroxiredoxin C, a member of the peroxiredoxin family of Arabidopsis thaliana: its expression and activity in comparison with other peroxiredoxins. Plant Physiol Biochem 40:491–499CrossRefGoogle Scholar
  45. Horling F, Lamkemeyer P, Konig J, Finkemeier I, Kandlbinder A, Baier M, Dietz K-J (2003) Divergent light-, ascorbate-, and oxidative stress-dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis. Plant Physiol 131:317–325CrossRefPubMedPubMedCentralGoogle Scholar
  46. Hu J, Baker A, Bartel B, Linka N, Mullen RT, Reumann S, Zolman BK (2012) Plant peroxisomes: biogenesis and function. Plant Cell 24:2279–2303CrossRefPubMedPubMedCentralGoogle Scholar
  47. Huang AHC, Trelease RN, Moore TS (1983) Plant peroxisomes. Academic Press, New YorkGoogle Scholar
  48. Igamberdiev AU, Lea PJ (2002) The role of peroxisomes in the integration of metabolism and evolutionary diversity of photosynthetic organisms. Phytochemistry 60:651–674CrossRefPubMedGoogle Scholar
  49. Immenschuh S, Baumgart-Vogt E, Tan M, Iwahara S, Ramadori G, Fahimi HD (2003) Differential cellular and subcellular localization of heme-binding protein 23/peroxiredoxin I and heme oxygenase-1 in rat liver. J Histochem Cytochem 51:1621–1631CrossRefPubMedGoogle Scholar
  50. Jiménez A, Hernández JA, del Río LA, Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284CrossRefPubMedPubMedCentralGoogle Scholar
  51. Kim SY, Paeng SK, Nawkar GM, Maibam P, Lee ES, Kim KS, Lee DH, Park DJ, Kang SB, Kim MR, Lee JH, Kim YH, Kim WY, Kang CH (2011) The 1-Cys peroxiredoxin, a regulator of seed dormancy, functions as a molecular chaperone under oxidative stress conditions. Plant Sci 181:119–124CrossRefPubMedGoogle Scholar
  52. Knoops B, Clippe A, Bogard C, Arsalane K, Wattiez R, Hermans C, Duconseille E, Falmagne P, Bernard A (1999) Cloning and characterization of AOEB166, a novel mammalian antioxidant enzyme of the peroxiredoxin family. J Biol Chem 274:30451–30458CrossRefPubMedGoogle Scholar
  53. Knoops B, Goemaere J, Van der Eecken V, Declercq JP (2011) Peroxiredoxin 5: structure, mechanism, and function of the mammalian atypical 2-Cys peroxiredoxin. Antioxid Redox Signal 15:817–829CrossRefPubMedGoogle Scholar
  54. Lamkemeyer P, Laxa M, Collin V, Li W, Finkemeier I, Schottler MA, Holtkamp V, Tognetti VB, Issakidis-Bourguet E, Kandlbinder A, Weis E, Miginiac-Maslow M, Dietz K-J (2006) Peroxiredoxin Q of Arabidopsis thaliana is attached to the thylakoids and functions in context of photosynthesis. Plant J 45:968–981CrossRefPubMedGoogle Scholar
  55. Lee EM, Lee SS, Tripathi BN, Jung HS, Cao GP, Lee Y, Singh S, Hong SH, Lee KW, Lee SY, Cho JY, Chung BY (2015) Site-directed 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 116:713–725CrossRefPubMedPubMedCentralGoogle Scholar
  56. Leterrier M, Corpas FJ, Barroso JB, Sandalio LM, del Río LA (2005) Peroxisomal monodehydroascorbate reductase: genomic clone characterization and functional analysis under environmental stress conditions. Plant Physiol 138:2111–2123CrossRefPubMedPubMedCentralGoogle Scholar
  57. López-Huertas E, del Río LA (2014) Characterization of antioxidant enzymes and peroxisomes of olive (Olea europaea L.) fruits. J Plant Physiol 171:1463–1471CrossRefPubMedGoogle Scholar
  58. López-Huertas E, Sandalio LM, del Río LA (1995) Integral membrane polypeptides of pea leaf peroxisomes: characterization and response to plant stress. Plant Physiol Biochem 33:295–302Google Scholar
  59. López-Huertas E, Corpas FJ, Sandalio LM, del Río LA (1999) Characterization of membrane polypeptides from pea leaf peroxisomes involved in superoxide radical generation. Biochem J 337:531–536CrossRefPubMedPubMedCentralGoogle Scholar
  60. McCarthy I, Romero-Puertas MC, Palma JM, Sandalio LM, Corpas FJ, Gómez M, del Río LA (2001) Cadmium induces senescence symptoms in leaf peroxisomes of pea plants. Plant Cell Environ 24:1065–1073CrossRefGoogle Scholar
  61. McCarthy I, Gómez M, del Río LA, Palma JM (2011) Role of peroxisomes in the oxidative injury induced by 2,4-dichlorophenoxyacetic acid in leaves of pea plants. Biol Plant 55:485–492CrossRefGoogle Scholar
  62. Minorsky PV (2002) Peroxisomes: organelles of diverse function. Plant Physiol 130:517–518CrossRefPubMedCentralGoogle Scholar
  63. Palma JM, Jiménez A, Sandalio LM, Corpas FJ, Lundqvist M, Gómez M, Sevilla F, del Río LA (2006) Antioxidative enzymes from chloroplasts, mitochondria, and peroxisomes during leaf senescence of nodulated pea plants. J Exp Bot 57:1747–1758CrossRefPubMedGoogle Scholar
  64. Park SG, Cha MK, Jeong W, Kim IH (2000) Distinct physiological functions of thiol peroxidase isoenzymes in Saccharomyces cerevisiae. J Biol Chem 275:5723–5732CrossRefPubMedGoogle Scholar
  65. Pedrajas JR, Miranda-Vizuete A, Javanmardy N, Gustafsson JA, Spyrou G (2000) Mitochondria of Saccharomyces cerevisiae contain one-conserved cysteine type peroxiredoxin with thioredoxin peroxidase activity. J Biol Chem 275:16296–16301CrossRefPubMedGoogle Scholar
  66. Pedrajas JR, McDonagh B, Hernández-Torres F, Miranda-Vizuete A, González-Ojeda R, Martínez-Galisteo E, Padilla CA, Bárcena JA (2016) Glutathione is the resolving thiol for thioredoxin peroxidase activity of 1-Cys peroxiredoxin without being consumed during the catalytic cycle. Antioxid Redox Signal 24:115–128CrossRefPubMedGoogle Scholar
  67. Reumann S, Weber AP (2006) Plant peroxisomes respire in the light: some gaps of the photorespiratory C2 cycle have become filled—others remain. Biochim Biophys Acta 1763:1496–1510CrossRefPubMedGoogle Scholar
  68. Reumann S, Babujee L, Ma C, Wienkoop S, Siemsen T, Antonicelli GE, Rasche N, Lüder F, Weckwerth W, Jahn O (2007) Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. Plant Cell 19:3170–3193CrossRefPubMedPubMedCentralGoogle Scholar
  69. Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, del Río LA, Sandalio LM (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29:1532–1544CrossRefPubMedGoogle Scholar
  70. Romero-Puertas MC, McCarthy I, Sandalio LM, Palma JM, Corpas FJ, Gómez M, del Río LA (1999) Cadmium toxicity and oxidative metabolism of pea leaf peroxisomes. Free Radic Res 31:S25–S31CrossRefPubMedGoogle Scholar
  71. Romero-Puertas MC, Rodríguez-Serrano M, Corpas FJ, Gómez M, del Río LA, Sandalio LM (2004a) Cadmium-induced subcellular accumulation of O2·− and H2O2 in pea leaves. Plant Cell Environ 27:1122–1134CrossRefGoogle Scholar
  72. Romero-Puertas MC, McCarthy I, Gómez M, Sandalio LM, Corpas FJ, del Río LA, Palma JM (2004b) Reactive oxygen species-mediated enzymatic systems involved in the oxidative action of 2,4-dichlorophenoxyacetic acid. Plant Cell Environ 27:1135–1148CrossRefGoogle Scholar
  73. Romero-Puertas MC, Corpas FJ, Sandalio LM, Leterrier M, Rodriguez-Serrano M, del Río LA, Palma JM (2006) Glutathione reductase from pea leaves: response to abiotic stress and characterization of the peroxisomal isozyme. New Phytol 170:43–52CrossRefPubMedGoogle Scholar
  74. Romero-Puertas MC, Laxa M, Mattè A, Zaninotto F, Finkemeier I, Jones AM, Perazzolli M, Vandelle E, Dietz KJ, Delledonne M (2007) S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell 19:4120–4130CrossRefPubMedPubMedCentralGoogle Scholar
  75. Rouhier N, Jacquot JP (2005) The plant multigenic family of thiol peroxidases. Free Radic Biol Med 38:1413–1421CrossRefPubMedGoogle Scholar
  76. Sakamoto A, Tsukamoto S, Yamamoto H, Ueda-Hashimoto M, Takahashi M, Suzuki H, Morikawa H (2003) Functional complementation in yeast reveals a protective role of chloroplast 2-Cys peroxiredoxin against reactive nitrogen species. Plant J 33:841–851CrossRefPubMedGoogle Scholar
  77. Sandalio LM, López-Huertas E, Bueno P, del Río LA (1997) Immunocytochemical localization of copper, zinc superoxide dismutase in peroxisomes from watermelon (Citrullus vulgaris Schrad.) cotyledons. Free Radic Res 26:187–194CrossRefPubMedGoogle Scholar
  78. Sandalio LM, Rodríguez-Serrano M, Romero-Puertas MC, del Río LA (2013) Role of peroxisomes as a source of reactive oxygen species (ROS) signalling molecules. Subcell Biochem 69:231–255CrossRefPubMedGoogle Scholar
  79. Seo MS, Kang SW, Kim K, Baines IC, Lee TH, Rhee SG (2000) Identification of a new type of mammalian peroxiredoxin that forms an intramolecular disulfide as a reaction intermediate. J Biol Chem 275:20346–20354CrossRefPubMedGoogle Scholar
  80. Sevilla F, Camejo D, Ortiz-Espín A, Calderón A, Lázaro JJ, Jiménez A (2015) The thioredoxin/peroxiredoxin/sulfiredoxin system: current overview on its redox function in plants and regulation by reactive oxygen and nitrogen species. J Exp Bot 66:2945–2955CrossRefPubMedGoogle Scholar
  81. Tabak HF, Braakman I, Distel B (1999) Peroxisomes: simple in function but complex in maintenance. Trends Cell Biol 9:447–453CrossRefPubMedGoogle Scholar
  82. Trujillo M, Ferrer-Sueta G, Thomson L, Flohé L, Radi R (2007) Kinetics of peroxiredoxins and their role in the decomposition of peroxynitrite. Subcell Biochem 44:83–113CrossRefPubMedGoogle Scholar
  83. Vernon LP (1960) Spectrophotometric determination of chlorophylls and pheophytins in plant extracts. Anal Chem 32:1144–1150CrossRefGoogle Scholar
  84. Walbrecq G, Wang B, Becker S, Hannotiau A, Fransen M, Knoops B (2015) Antioxidant cytoprotection by peroxisomal peroxiredoxin-5. Free Radic Biol Med 84:215–226CrossRefPubMedGoogle Scholar
  85. Walk R, Hock B (1977) Glyoxysomal malate dehydrogenase of watermelon cotyledons: de novo synthesis of cytoplasmic ribosomes. Planta 134:277–285CrossRefPubMedGoogle Scholar
  86. Wood ZA, Schröder E, Harris JR, Poole LB (2003) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci 28:32–40CrossRefPubMedGoogle Scholar
  87. Yamaguchi K, Mori H, Nishimura M (1995) A novel isoenzyme of ascorbate peroxidase localized on glyoxysomal and leaf peroxisomal membranes in pumpkin. Plant Cell Physiol 36:1157–1162PubMedGoogle Scholar
  88. Yamashita H, Avraham S, Jiang S, London R, Van Veldhoven PP, Subramani S, Rogers RA, Avraham H (1999) Characterization of human and murine PMP20 peroxisomal proteins that exhibit antioxidant activity in vitro. J Biol Chem 274:29897–29904CrossRefPubMedGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2017

Authors and Affiliations

  • Francisco J. Corpas
    • 1
    Email author
  • José R. Pedrajas
    • 2
  • José M. Palma
    • 1
  • Raquel Valderrama
    • 2
  • Marta Rodríguez-Ruiz
    • 1
  • Mounira Chaki
    • 2
  • Luis A. del Río
    • 1
  • Juan B. Barroso
    • 2
  1. 1.Group of Antioxidants, Free Radicals and Nitric Oxide in Biotechnology, Food and Agriculture, Department of Biochemistry, Cell and Molecular Biology of PlantsEstación Experimental del Zaidín, CSICGranadaSpain
  2. 2.Group of Biochemistry and Cell Signaling in Nitric Oxide, Department of Biochemistry and Molecular BiologyUniversity of JaénJaénSpain

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