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Hydrogen Peroxide (H2O2)- and Nitric Oxide (NO)-Derived Posttranslational Modifications

  • R. Valderrama
  • J. C. Begara-Morales
  • M. Chaki
  • C. Mata-Pérez
  • M. N. Padilla
  • J. B. BarrosoEmail author
Chapter

Abstract

Posttranslational modifications (PTMs) of proteins can be considered an additional step in protein metabolism that greatly expands the proteome of living organisms. In plant systems, PTMs affect protein structure and activity which are associated with concomitant changes in signaling and gene expression that make cellular systems more dynamic.

Redox reactions, which are a very old signaling phenomenon in evolutionarily terms, occur in prokaryotes and eukaryotes. The most important redox molecules are reactive oxygen species (ROS), such as singlet oxygen (1O2), hydroxyl radical (·OH), superoxide anion (O2·−), and hydrogen peroxide (H2O2), as well as reactive nitrogen species (RNS) such as nitric oxide (NO) and derived compounds. H2O2 and NO are essential signaling molecules involved in many physiological processes and plant responses to unfavorable conditions. These diverse functions can be partly explained by the fact that ROS and NO rapidly interact to form a number of reactive nitrogen species, such as peroxynitrite (ONOO), nitrogen dioxide (NO2), dinitrogen trioxide (N2O3), and other NOx species. Moreover, as these molecules share signaling pathways, it is not surprising that cross talk enables pathways to control each other’s functions.

In this chapter, we will explore up-to-date knowledge concerning the effects of H2O2- and NO-derived PTMs such as carbonylation, sulfhydryl oxidations, nitration, S-nitrosylation, and nitroalkylation while emphasizing in the importance of the interplay between their signaling pathways in plant systems.

Keywords

Hydrogen peroxide (H2O2Nitric oxide (NO) Posttranslational modifications (PTMs) Carbonylation Sulfhydryl oxidation Nitration S-nitrosylation Nitroalkylation 

Notes

Acknowledgments

Work in our laboratory are funded by an ERDF-cofinanced grant from the Spanish Ministry of Economy and Competitiveness (project BIO2015-66390-P; MINECO/FEDER) and the Junta de Andalucía (group BIO286).

References

  1. Abat JK, Deswal R (2009) Differential modulation of S-nitrosoproteome of Brassica juncea by low temperature: change in S-nitrosylation of Rubisco is responsible for the inactivation of its carboxylase activity. Proteomics 9:4368–4380PubMedCrossRefGoogle Scholar
  2. Abe K, Kimura H (1996) The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16:1066–1071PubMedCrossRefGoogle Scholar
  3. Abello N, Kerstjens HAM, Postma DS, Bischoff R (2009) Protein tyrosine nitration: selectivity, physicochemical and biological consequences, denitration, and proteomics methods for the identification of tyrosine-nitrated proteins. J Proteome Res 8:3222–3238PubMedCrossRefGoogle Scholar
  4. Airaki M, Leterrier M, Mateos RM, Valderrama R, Chaki M, Barroso JB, del Río LA, Palma JM, Corpas FJ (2012) Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant Cell Environ 35:281–295PubMedCrossRefGoogle Scholar
  5. Akter S, Huang J, Waszczak C, Jacques S, Gevaert K, Van Breusegem F, Messens J (2015) Cysteines under ROS attack in plants: a proteomics view. J Exp Bot 66:2935–2944PubMedCrossRefGoogle Scholar
  6. Albertos P, Romero-Puertas MC, Tatematsu K, Mateos I, Sánchez-Vicente I, Nambara E, Lorenzo O (2015) S-nitrosylation triggers ABI5 degradation to promote seed germination and seedling growth. Nat Commun 6:8669PubMedPubMedCentralCrossRefGoogle Scholar
  7. Anand P, Stamler JS (2012) Enzymatic mechanisms regulating protein s-nitrosylation: implications in health and disease. J Mol Med 90:233–244PubMedPubMedCentralCrossRefGoogle Scholar
  8. Arc E, Galland M, Cueff G, Godin B, Lounifi I, Job D, Rajjou L (2011) Reboot the system thanks to protein post-translational modifications and proteome diversity: how quiescent seeds restart their metabolism to prepare seedling establishment. J Proteome 11:1606–1618CrossRefGoogle Scholar
  9. Aroca Á, Serna A, Gotor C, Romero LC (2015) S-Sulfhydration: a cysteine posttranslational modification in plant systems. Plant Physiol 168:334–342PubMedPubMedCentralCrossRefGoogle Scholar
  10. Astier J, Rasul S, Koen E, Manzoor H, Besson-Bard A, Lamotte O, Jeandroz S, Durner J, Lindermayr C (2011) S-nitrosylation: an emerging post-translational protein modification in plants. Plant Sci 181:527–533PubMedCrossRefPubMedCentralGoogle Scholar
  11. Bai X, Yang L, Tian M, Chen J, Shi J, Yang Y, Hu X (2011) Nitric Oxide enhances desiccation tolerance of recalcitrant antiaris toxicaria seeds via protein S-nitrosylation and carbonylation. PLoS One 6:e20714PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bai XG, Chen JH, Kong XX, Todd CD, Yang YP, Hu XY, Li DZ (2012) Carbon monoxide enhances the chilling tolerance of recalcitrant Baccaurea ramiflora seeds via nitric oxide-mediated glutathione homeostasis. Free Radic Biol Med 53:710–720PubMedCrossRefGoogle Scholar
  13. Baker PRS, Schopfer FJ, Sweeney S, Freeman B (2004) Red cell membrane and plasma linoleic acid nitration products: synthesis, clinical identification, and quantitation. Proc Natl Acad Sci U S A 101:11577–11582PubMedPubMedCentralCrossRefGoogle Scholar
  14. Baker LMS, Baker PRS, Golin-Bisello F, Schopfer FJ, Fink M, Woodcock SR, Branchaud BP, Radi R, Freeman BA (2007) Nitro-fatty acid reaction with glutathione and cysteine: kinetic analysis of thiol alkylation by a Michael addition reaction. J Biol Chem 282:31085–31093PubMedPubMedCentralCrossRefGoogle Scholar
  15. Barroso JB, Corpas FJ, Carreras A, Sandalio LM, Valderrama R, Palma JM, Lupiánez JA, Del Río LA (1999) Localization of nitric-oxide synthase in plant peroxisomes. J Biol Chem 274:36729–36733PubMedCrossRefPubMedCentralGoogle Scholar
  16. Barroso JB, Corpas FJ, Carreras A, Rodríguez-Serrano M, Esteban FJ, Fernández-Ocaña A, Chaki M, Romero-Puertas MC, Valderrama R, Sandalio LM, del Río LA (2006) Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. J Exp Bot 57:1785–1793PubMedCrossRefPubMedCentralGoogle Scholar
  17. Batthyany C, Schopfer FJ, Baker PRS, Durán R, Baker LMS, Huang Y, Cerveñansky C, Branchaud BP, Freeman BA (2006) Reversible post-translational modification of proteins by nitrated fatty acids in vivo. J Biol Chem 281:20450–20463PubMedPubMedCentralCrossRefGoogle Scholar
  18. Bedhomme M, Adamo M, Marchand CH, Couturier J, Rouhier N, Lemaire SD, Zaffagnini M, Trost P (2012) Glutathionylation of cytosolic glyceraldehyde-3-phosphate dehydrogenase from the model plant Arabidopsis thaliana is reversed by both glutaredoxins and thioredoxins in vitro. Biochem J 445:337–347PubMedCrossRefGoogle Scholar
  19. Begara-Morales JC, Chaki M, Sánchez-Calvo B, Mata-Pérez C, Leterrier M, Palma JM, Barroso JB, Corpas FJ (2013a) Protein tyrosine nitration in pea roots during development and senescence. J Exp Bot 64:1121–1134PubMedPubMedCentralCrossRefGoogle Scholar
  20. Begara-Morales JC, López-Jaramillo FJ, Sánchez-Calvo B, Carreras A, Ortega-Muñoz M, Santoyo-González F, Corpas FJ, Barroso JB (2013b) Vinyl sulfone silica: application of an open preactivated support to the study of transnitrosylation of plant proteins by S-nitrosoglutathione. BMC Plant Biol 13:61PubMedPubMedCentralCrossRefGoogle Scholar
  21. Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, López-Jaramillo J, Padilla MN, Carreras A, Corpas FJ, Barroso JB (2014) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J Exp Bot 65:527–538PubMedCrossRefGoogle Scholar
  22. Begara-Morales JC, Sánchez-Calvo B, Chaki M, Mata-Pérez C, Valderrama R, Padilla MN, López-Jaramillo J, Luque F, Corpas FJ, Barroso JB (2015) Differential molecular response of monodehydroascorbate reductase and glutathione reductase by nitration and S-nitrosylation. J Exp Bot 66:5983–5996PubMedPubMedCentralCrossRefGoogle Scholar
  23. Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, Corpas FJ, Barroso JB (2016a) Protein S-nitrosylation and S-glutathionylation as regulators of redox homeostasis during abiotic stress response. In: Gupta DK, Palma JM, Corpas FJ (eds) Redox state as a central regulator of plant-cell stress responses. Springer, Cham, pp 365–386CrossRefGoogle Scholar
  24. Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, Padilla MN, Corpas FJ, Barroso JB (2016b) Antioxidant systems are regulated by nitric oxide-mediated post-translational modifications (NO-PTMs). Front Plant Sci 7:152PubMedPubMedCentralCrossRefGoogle Scholar
  25. Begara-Morales JC, Chaki M, Valderrama R, Sánchez-Calvo B, Mata-Pérez C, Padilla MN, Corpas FJ, Barroso JB (2018) Nitric oxide buffering and conditional nitric oxide release in stress response. J Exp Bot 69:3425–3438PubMedCrossRefGoogle Scholar
  26. Belenghi B, Romero-Puertas MC, Vercammen D, Brackenier A, Inzé D, Delledonne M, Van Breusegem F (2007) Metacaspase activity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cysteine residue. J Biol Chem 282:1352–1358PubMedCrossRefGoogle Scholar
  27. Benhar M, Forrester MT, Hess DT, Stamler JS (2008) Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science 320:1050–1054PubMedPubMedCentralCrossRefGoogle Scholar
  28. Benhar M, Forrester MT, Stamler JS (2009) Protein denitrosylation: enzymatic mechanisms and cellular functions. Nat Rev Mol Cell Biol 10:721–732PubMedCrossRefGoogle Scholar
  29. Biteau B, Labarre J, Toledano MB (2003) ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425:980–984PubMedCrossRefGoogle Scholar
  30. Boschi-Muller S, Gand A, Branlant G (2008) The methionine sulfoxide reductases: catalysis and substrate specificities. Arch Biochem Biophys 474:266–273PubMedCrossRefGoogle Scholar
  31. Broniowska KA, Diers AR, Hogg N (2013) S-Nitrosoglutathione. Biochim Biophys Acta 1830:3173–3181PubMedPubMedCentralCrossRefGoogle Scholar
  32. Camejo D, Romero-Puertas MC, Rodríguez-Serrano M, Sandalio LM, Lázaro JJ, Jiménez A, Sevilla F (2013) Salinity-induced changes in S-nitrosylation of pea mitochondrial proteins. J Proteome 79:87–99CrossRefGoogle Scholar
  33. Camejo D, Ortiz-Espín A, Lázaro JJ, Romero-Puertas MC, Lázaro-Payo A, Sevilla F, Jiménez A (2015) Functional and structural changes in plant mitochondrial PrxII F caused by NO. J Proteome 119:112–125CrossRefGoogle Scholar
  34. Castillo MC, Lozano-Juste J, González-Guzmán M, Rodriguez L, Rodriguez PL, León J (2015) Inactivation of PYR/PYL/RCAR ABA receptors by tyrosine nitration may enable rapid inhibition of ABA signaling by nitric oxide in plants. Sci Signal 8:ra89CrossRefGoogle Scholar
  35. Chaki M, Fernández-Ocaña AM, Valderrama R, Carreras A, Esteban FJ, Luque F, Gómez-Rodríguez MV, Begara-Morales JC, Corpas FJ, Barroso JB (2009a) Involvement of reactive nitrogen and oxygen species (RNS and ROS) in sunflower-mildew interaction. Plant Cell Physiol 50:265–279PubMedCrossRefPubMedCentralGoogle Scholar
  36. Chaki M, Valderrama R, Fernández-Ocaña AM, Carreras A, López-Jaramillo J, Luque F, Palma JM, Pedrajas JR, Begara-Morales JC, Sánchez-Calvo B, Gómez-Rodríguez MV, Corpas FJ, Barroso JB (2009b) Protein targets of tyrosine nitration in sunflower (Helianthus annuus L.) hypocotyls. J Exp Bot 60:4221–4234PubMedCrossRefPubMedCentralGoogle Scholar
  37. Chaki M, Valderrama R, Fernández-Ocaña AM, Carreras A, Gómez-Rodríguez MV, Pedrajas JR, Begara-Morales JC, Sánchez-Calvo B, Luque F, Leterrier M, Corpas FJ, Barroso JB (2011a) Mechanical wounding induces a nitrosative stress by down-regulation of GSNO reductase and an increase in S-nitrosothiols in sunflower (Helianthus annuus) seedlings. J Exp Bot 62:1803–1813PubMedCrossRefPubMedCentralGoogle Scholar
  38. Chaki M, Valderrama R, Fernández-Ocaña AM, Carreras A, Gómez-Rodríguez MV, López-Jaramillo J, Begara-Morales JC, Sánchez-Calvo B, Luque F, Leterrier M, Corpas FJ, Barroso JB (2011b) High temperature triggers the metabolism of S-nitrosothiols in sunflower mediating a process of nitrosative stress which provokes the inhibition of ferredoxin-NADP reductase by tyrosine nitration. Plant Cell Environ 34:1803–1818PubMedCrossRefGoogle Scholar
  39. 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 116:637–647PubMedPubMedCentralCrossRefGoogle Scholar
  40. Corpas FJ, Barroso J (2004) Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiol 136:2722–2733PubMedPubMedCentralCrossRefGoogle Scholar
  41. Corpas FJ, Barroso JB (2013) Nitro-oxidative stress vs oxidative or nitrosative stress in higher plants. New Phytol 199:633–635PubMedCrossRefGoogle Scholar
  42. Corpas FJ, Barroso JB (2015) Nitric oxide from a “green” perspective. Nitric Oxide Biol Chem 45:15–19CrossRefGoogle Scholar
  43. Corpas FJ, Barroso JB (2017) Nitric oxide synthase-like activity in higher plants. Nitric Oxide 68:5–6PubMedCrossRefPubMedCentralGoogle Scholar
  44. Corpas FJ, Barroso JB, del Río LA (2004) Enzymatic sources of nitric oxide in plant cells – beyond one protein-one function. New Phytol 162:243–251CrossRefGoogle Scholar
  45. Corpas FJ, Chaki M, Fernández-Ocaña A, Valderrama R, Palma JM, Carreras A, Begara-Morales JC, Airaki M, del Río LA, Barroso JB (2008) Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol 49:1711–1722PubMedCrossRefGoogle Scholar
  46. Corpas FJ, Palma JM, Del Rio L, Barroso JB (2009) Evidence supporting the existence of l-arginine-dependent nitric oxide synthase activity in plants. New Phytol 184:9–14PubMedCrossRefPubMedCentralGoogle Scholar
  47. Corpas FJ, Leterrier M, Begara-Morales JC, Valderrama R, Chaki M, López-Jaramillo J, Luque F, Palma JM, Padilla MN, Sánchez-Calvo B, Mata-Pérez C, Barroso JB (2013) Inhibition of peroxisomal hydroxypyruvate reductase (HPR1) by tyrosine nitration. Biochim Biophys Acta 1830:4981–4989PubMedCrossRefGoogle Scholar
  48. Dalle-Donne I, Rossi R, Giustarini D, Gagliano N, Lusini L, Milzani A, Di Simplicio P, Colombo R (2001) Actin carbonylation: from a simple marker of protein oxidation to relevant signs of severe functional impairment. Free Radic Biol Med 31:1075–1083PubMedCrossRefGoogle Scholar
  49. Dalle-Donne I, Rossi R, Giustarini D, Colombo R, Milzani A (2007) S-glutathionylation in protein redox regulation. Free Radic Biol Med 43:883–898PubMedCrossRefGoogle Scholar
  50. Damiani I, Pauly N, Puppo A, Brouquisse R, Boscari A (2016) Reactive oxygen species and nitric oxide control early steps of the legume – rhizobium symbiotic interaction. Front Plant Sci 7:454PubMedPubMedCentralGoogle Scholar
  51. Dat JF, Inze D, van Breusegem F (2001) Catalase-deficient tobacco plants: tools for in planta studies on the role of hydrogen peroxide. Redox Rep 6:37–42PubMedCrossRefGoogle Scholar
  52. Davies MJ (2005) The oxidative environment and protein damage. Biochim Biophys Acta 1703:93–109PubMedCrossRefGoogle Scholar
  53. Deeb RS, Nuriel T, Cheung C, Summers B, Lamon BD, Gross SS, Hajjar DP (2013) Characterization of a cellular denitrase activity that reverses nitration of cyclooxygenase. AJP Hear Circ Physiol 305:H687–H698CrossRefGoogle Scholar
  54. Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci U S A 98:13454–13459PubMedPubMedCentralCrossRefGoogle Scholar
  55. Dietz KJ (2014) Redox regulation of transcription factors in plant stress acclimation and development. Antioxid Redox Signal 21:1356–1372PubMedCrossRefGoogle Scholar
  56. Dixon DP, Davis BG, Edwards R (2002) Functional divergence in the glutathione transferase superfamily in plants: Identification of two classes with putative functions in redox homeostasis in Arabidopsis thaliana. J Biol Chem 277:30859–30869PubMedCrossRefGoogle Scholar
  57. Dixon DP, Skipsey M, Grundy NM, Edwards R (2005) Stress-induced protein S-glutathionylation in arabidopsis. Plant Physiol 138:2233–2244PubMedPubMedCentralCrossRefGoogle Scholar
  58. Durner J, Gow AJ, Stamler JS, Glazebrook J (1999) Ancient origins of nitric oxide signaling in biological systems. Proc Natl Acad Sci U S A 96:14206–14207PubMedPubMedCentralCrossRefGoogle Scholar
  59. El-Maarouf-Bouteau H, Bailly C (2008) Oxidative signaling in seed germination and dormancy. Plant Signal Behav 3:175–182PubMedPubMedCentralCrossRefGoogle Scholar
  60. Fares A, Rossignol M, Peltier JB (2011) Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochem Biophys Res Commun 416:331–336PubMedCrossRefGoogle Scholar
  61. Farnese FS, Menezes-Silva PE, Gusman GS, Oliveira JA (2016) When bad guys become good ones: the key role of reactive oxygen species and nitric oxide in the plant responses to abiotic stress. Front Plant Sci 7:471PubMedPubMedCentralCrossRefGoogle Scholar
  62. Fazzari M, Trostchansky A, Schopfer FJ, Salvatore SR, Sánchez-Calvo B, Vitturi D, Valderrama R, Barroso JB, Radi R, Freeman BA, Rubbo H (2014) Olives and olive oil are sources of electrophilic fatty acid nitroalkenes. PLoS One 9(1):e84884PubMedPubMedCentralCrossRefGoogle Scholar
  63. Feechan A, Kwon E, Yun BW, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. Proc Natl Acad Sci U S A 102:8054–8059PubMedPubMedCentralCrossRefGoogle Scholar
  64. Feigl G, Kolbert Z, Lehotai N, Molnár Á, Ördög A, Bordé Á, Laskay G, Erdei L (2016) Different zinc sensitivity of Brassica organs is accompanied by distinct responses in protein nitration level and pattern. Ecotoxicol Environ Saf 125:141–152PubMedCrossRefGoogle Scholar
  65. Foyer CH, Noctor G (2016) Stress-triggered redox signalling: what’s in pROSpect? Plant Cell Environ 39:951–964PubMedCrossRefPubMedCentralGoogle Scholar
  66. Foyer CH, Ruban AV, Noctor G (2017) Viewing oxidative stress through the lens of oxidative signalling rather than damage. Biochem J 474:877–883PubMedPubMedCentralCrossRefGoogle Scholar
  67. Freeman BA, Baker PRS, Schopfer FJ, Woodcock SR, Napolitano A, D’Ischia M (2008) Nitro-fatty acid formation and signaling. J Biol Chem 283:15515–15519PubMedPubMedCentralCrossRefGoogle Scholar
  68. Friso G, van Wijk KJ (2015) Update: post-translational protein modifications in plant metabolism. Plant Physiol 169:1469–1487PubMedPubMedCentralGoogle Scholar
  69. Frungillo L, Skelly MJ, Loake GJ, Spoel SH, Salgado I (2014) S-nitrosothiols regulate nitric oxide production and storage in plants through the nitrogen assimilation pathway. Nat Commun 5:1–10CrossRefGoogle Scholar
  70. Fukuto JM, Carrington SJ, Tantillo DJ, Harrison JG, Ignarro LJ, Freeman BA, Chen A, Wink DA (2012) Small molecule signaling agents: the integrated chemistry and biochemistry of nitrogen oxides, oxides of carbon, dioxygen, hydrogen sulfide, and their derived species. Chem Res Toxicol 25:769–793PubMedPubMedCentralCrossRefGoogle Scholar
  71. Gallogly MM, Mieyal JJ (2007) Mechanisms of reversible protein glutathionylation in redox signaling and oxidative stress. Curr Opin Pharmacol 7:381–391PubMedCrossRefGoogle Scholar
  72. Gao XH, Bedhomme M, Veyel D, Zaffagnini M, Lemaire SD (2009) Methods for analysis of protein glutathionylation and their application to photosynthetic organisms. Mol Plant 2:218–235PubMedCrossRefGoogle Scholar
  73. Gaston B, Reilly J, Drazen JM, Fackler J, Ramdev P, Arnelle D, Mullins ME, Sugarbaker DJ, Chee C, Singel DJ (1993) Endogenous nitrogen oxides and bronchodilator S-nitrosothiols in human airways. Proc Natl Acad Sci U S A 90:10957–10961PubMedPubMedCentralCrossRefGoogle Scholar
  74. Geisler AC, Rudolph TK (2012) Nitroalkylation – a redox sensitive signaling pathway. Biochim Biophys Acta 1820:777–784PubMedCrossRefGoogle Scholar
  75. Gong YW, Yuan YJ (2006) Nitric oxide mediates inactivation of glutathione S-transferase in suspension culture of Taxus cuspidata during shear stress. J Biotechnol 123:185–192PubMedCrossRefGoogle Scholar
  76. Görg B, Qvartskhava N, Voss P, Grune T, Häussinger D, Schliess F (2007) Reversible inhibition of mammalian glutamine synthetase by tyrosine nitration. FEBS Lett 581:84–90PubMedCrossRefGoogle Scholar
  77. Gow AJ, Farkouh CR, Munson DA, Posencheg MA, Ischiropoulos H (2004) Biological significance of nitric oxide-mediated protein modifications. Am J Phys Lung Cell Mol Phys 287:L262–L268Google Scholar
  78. Gruhlke MCH, Slusarenko AJ (2012) The biology of reactive sulfur species (RSS). Plant Physiol Biochem 59:98–107PubMedCrossRefGoogle Scholar
  79. Habibi G (2014) Hydrogen peroxide (H2O2) generation, scavenging and signaling in plants. In: Ahmad P (ed) Oxidative damage to plants: antioxidant networks and signaling. Academic Press, Amsterdam, pp 557–584CrossRefGoogle Scholar
  80. Haque A, Andersen JN, Salmeen A, Barford D, Tonks NK (2011) Conformation-sensing antibodies stabilize the oxidized form of PTP1B and inhibit its phosphatase activity. Cell 147:185–198PubMedPubMedCentralCrossRefGoogle Scholar
  81. Harris TK, Turner GJ (2002) Structural basis of perturbed pK a values of catalytic groups in enzyme active sites. IUBMB Life 53:85–98PubMedCrossRefGoogle Scholar
  82. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS (2005) Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6:150–166PubMedCrossRefGoogle Scholar
  83. Hiscock SJ, Bright J, McInnis SM, Desikan R, Hancock JT (2007) Signaling on the stigma: potential new roles for ROS and NO in plant cell signaling. Plant Signal Behav 2:23–24PubMedPubMedCentralCrossRefGoogle Scholar
  84. Holtgrefe S, Gohlke J, Starmann J, Druce S, Klocke S, Altmann B, Wojtera J, Lindermayr C, Scheibe R (2008) Regulation of plant cytosolic glyceraldehyde 3-phosphate dehydrogenase isoforms by thiol modifications. Physiol Plant 133:211–228PubMedCrossRefGoogle Scholar
  85. Holzmeister C, Gaupels F, Geerlof A, Sarioglu H, Sattler M, Durner J, Lindermayr C (2015) Differential inhibition of Arabidopsis superoxide dismutases by peroxynitrite-mediated tyrosine nitration. J Exp Bot 66:989–999PubMedCrossRefGoogle Scholar
  86. Hu J, Huang X, Chen L, Sun X, Lu C, Zhang L, Wang Y, Zuo J (2015) Site-specific nitrosoproteomic identification of endogenously S-Nitrosylated proteins in Arabidopsis. Plant Physiol 167:1731–1746PubMedPubMedCentralCrossRefGoogle Scholar
  87. Huber SC, Hardin SC (2004) Numerous posttranslational modifications provide opportunities for the intricate regulation of metabolic enzymes at multiple levels. Curr Opin Plant Biol 7:318–322PubMedCrossRefGoogle Scholar
  88. Jacques S, Ghesquière B, De Bock PJ, Demol H, Wahni K, Willems P, Messens J, Van Breusegem F, Gevaert K (2015) Protein methionine sulfoxide dynamics in Arabidopsis thaliana under oxidative stress. Mol Cell Proteomics 14:1217–1229PubMedPubMedCentralCrossRefGoogle Scholar
  89. Jain K, Siddam A, Marathi A, Roy U, Falck JR, Balazy M (2008) The mechanism of oleic acid nitration by ·NO2. Free Radic Biol Med 45:269–283PubMedCrossRefGoogle Scholar
  90. Jasid S, Simontacchi M, Bartoli CG, Puntarulo S (2006) Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins. Plant Physiol 142:1246–1255PubMedPubMedCentralCrossRefGoogle Scholar
  91. Job C, Rajjou L, Lovigny Y, Belghazi M, Job D (2005) Patterns of protein oxidation in Arabidopsis seeds and during germination. Plant Physiol 138:790–802PubMedPubMedCentralCrossRefGoogle Scholar
  92. Johansson E, Olsson O, Nyström T (2004) Progression and specificity of protein oxidation in the life cycle of Arabidopsis thaliana. J Biol Chem 279:22204–22208PubMedCrossRefGoogle Scholar
  93. Joudoi T, Shichiri Y, Kamizono N, Akaike T, Sawa T, Yoshitake J, Yamada N, Iwai S (2013) Nitrated cyclic GMP modulates guard cell signaling in Arabidopsis. Plant Cell 25:558–571PubMedPubMedCentralCrossRefGoogle Scholar
  94. Kabil O, Banerjee R (2010) Redox biochemistry of hydrogen sulfide. J Biol Chem 285:21903–21907PubMedPubMedCentralCrossRefGoogle Scholar
  95. Kato H, Takemoto D, Kawakita K (2013) Proteomic analysis of S-nitrosylated proteins in potato plant. Physiol Plant 148:371–386PubMedCrossRefGoogle Scholar
  96. Kitajima S, Kurioka M, Yoshimoto T, Shindo M, Kanaori K, Tajima K, Oda K (2008) A cysteine residue near the propionate side chain of heme is the radical site in ascorbate peroxidase. FEBS J 275:470–480PubMedCrossRefGoogle Scholar
  97. Kneeshaw S, Spoel SH (2018) Thioredoxin-dependent decomposition of protein S-nitrosothiols. Method Mol Biol 1747:281–297CrossRefGoogle Scholar
  98. Kneeshaw S, Gelineau S, Tada Y, Loake GJ, Spoel SH (2014) Selective protein denitrosylation activity of thioredoxin-h5 modulates plant immunity. Mol Cell 56:153–162PubMedCrossRefGoogle Scholar
  99. Kolluru GK, Shen X, Bir SC, Kevil CG (2013) Hydrogen sulfide chemical biology: pathophysiological roles and detection. Nitric Oxide 35:5–20PubMedPubMedCentralCrossRefGoogle Scholar
  100. Kovacs I, Holzmeister C, Wirtz M, Geerlof A, Fröhlich T, Römling G, Kuruthukulangarakoola GT, Linster E, Hell R, Arnold GJ, Durner J, Lindermayr C (2016) ROS-mediated inhibition of S-nitrosoglutathione reductase contributes to the activation of anti-oxidative mechanisms. Front Plant Sci 7:1669PubMedPubMedCentralCrossRefGoogle Scholar
  101. Krishnan N, Fu C, Pappin DJ, Tonks NK (2011) H2S-induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response. Sci Signal 4:ra86–ra86PubMedPubMedCentralCrossRefGoogle Scholar
  102. Lee JW, Helmann JD (2006) The PerR transcription factor senses H2O2 by metal-catalysed histidine oxidation. Nature 440:363–367PubMedCrossRefGoogle Scholar
  103. Leitner M, Vandelle E, Gaupels F, Bellin D, Delledonne M (2009) NO signals in the haze: nitric oxide signalling in plant defence. Curr Opin Plant Biol 12:451–458PubMedCrossRefGoogle Scholar
  104. Leterrier M, Chaki M, Airaki M, Valderrama R, Palma JM, Barroso JB, Corpas FJ (2011) Function of S-nitrosoglutathione reductase (GSNOR) in plant development and under biotic/abiotic stress. Plant Signal Behav 6:789–793PubMedPubMedCentralCrossRefGoogle Scholar
  105. Leterrier M, Airaki M, Palma JM, Chaki M, Barroso JB, Corpas FJ (2012) Arsenic triggers the nitric oxide (NO) and S-nitrosoglutathione (GSNO) metabolism in Arabidopsis. Environ Pollut 166:136–143PubMedCrossRefGoogle Scholar
  106. Leymarie J, Vitkauskaité G, Hoang HH, Gendreau E, Chazoule V, Meimoun P, Corbineau F, El-Maarouf-Bouteau H, Bailly C (2012) Role of reactive oxygen species in the regulation of Arabidopsis seed dormancy. Plant Cell Physiol 53:96–106PubMedCrossRefGoogle Scholar
  107. Li L, Rose P, Moore PK (2011) Hydrogen sulfide and cell signaling. Annu Rev Pharmacol Toxicol 51:169–187PubMedCrossRefGoogle Scholar
  108. Li CW, Lee SH, Chieh PS, Lin CS, Wang YC, Chan MT (2012) Arabidopsis root-abundant cytosolic methionine sulfoxide reductase B genes MsrB7 and MsrB8 are involved in tolerance to oxidative stress. Plant Cell Physiol 53:1707–1719PubMedCrossRefGoogle Scholar
  109. Lin A, Wang Y, Tang J, Xue P, Li C, Liu L, Hu B, Yang F, Loake GJ, Chu C (2012) Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice. Plant Physiol 158:451–464PubMedCrossRefPubMedCentralGoogle Scholar
  110. Lindermayr C (2018) Crosstalk between reactive oxygen species and nitric oxide in plants: key role of S-nitrosoglutathione reductase. Free Radic Biol Med 122:110–115PubMedCrossRefGoogle Scholar
  111. Lindermayr C, Durner J (2009) S-Nitrosylation in plants: pattern and function. J Proteome 73:1–9CrossRefGoogle Scholar
  112. Lindermayr C, Durner J (2015) Interplay of reactive oxygen species and nitric oxide: nitric oxide coordinates reactive oxygen species homeostasis. Plant Physiol 167:1209–1210PubMedPubMedCentralCrossRefGoogle Scholar
  113. Liu L, Hausladen A, Zeng M, Que L, Heitman J, Stamler JS (2001) A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410:490–494PubMedCrossRefGoogle Scholar
  114. Lounifi I, Arc E, Molassiotis A, Job D, Rajjou L, Tanou G (2013) Interplay between protein carbonylation and nitrosylation in plants. J Proteome 13:568–578CrossRefGoogle Scholar
  115. Lozano-Juste J, León J (2010) Enhanced abscisic acid-mediated responses in nia1nia2noa1-2 triple mutant impaired in NIA/NR- and AtNOA1-dependent nitric oxide biosynthesis in Arabidopsis. Plant Physiol 152:891–903PubMedPubMedCentralCrossRefGoogle Scholar
  116. Lozano-Juste J, Colom-Moreno R, León J (2011) In vivo protein tyrosine nitration in Arabidopsis thaliana. J Exp Bot 62:3501–3517PubMedPubMedCentralCrossRefGoogle Scholar
  117. Luo D, Smith SW, Anderson BD (2005) Kinetics and mechanism of the reaction of cysteine and hydrogen peroxide in aqueous solution. J Pharm Sci 94:304–316PubMedCrossRefGoogle Scholar
  118. Malik SI, Hussain A, Yun BW, Spoel SH, Loake GJ (2011) GSNOR-mediated de-nitrosylation in the plant defence response. Plant Sci 181:540–544PubMedCrossRefGoogle Scholar
  119. Marino SM, Gladyshev VN (2010) Cysteine function governs its conservation and degeneration and restricts its utilization on protein surfaces. J Mol Biol 404:902–916PubMedPubMedCentralCrossRefGoogle Scholar
  120. Mata-Pérez C, Sánchez-Calvo B, Begara-Morales JC, Carreras A, Padilla MN, Melguizo M, Valderrama R, Corpas FJ, Barroso JB (2016a) Nitro-linolenic acid is a nitric oxide donor. Nitric Oxide 57:57–63PubMedCrossRefGoogle Scholar
  121. Mata-Pérez C, Sánchez-Calvo B, Begara-Morales JC, Padilla MN, Valderrama R, Corpas FJ, Barroso JB (2016b) Nitric oxide release from nitro-fatty acids in Arabidopsis roots. Plant Signal Behav 11(3):e1154255PubMedPubMedCentralCrossRefGoogle Scholar
  122. Mata-Pérez C, Sánchez-Calvo B, Padilla MN, Begara-Morales JC, Luque F, Melguizo M, Jiménez-Ruiz J, Fierro-Risco J, Peñas-Sanjuán A, Valderrama R, Corpas FJ, Barroso JB (2016c) Nitro-fatty acids in plant signaling: nitro-linolenic acid induces the molecular chaperone network in Arabidopsis. Plant Physiol 170:686–701PubMedCrossRefGoogle Scholar
  123. Mata-Perez C, Begara-Morales JC, Chaki M, Sánchez-Calvo B, Valderrama R, Padilla MN, Corpas FJ, Barroso JB (2016d) Protein tyrosine nitration during development and abiotic stress response in plants. Front Plant Sci 7:1699PubMedPubMedCentralCrossRefGoogle Scholar
  124. Mata-Pérez C, Sánchez-Calvo B, Padilla MN, Begara-Morales JC, Valderrama R, Corpas FJ, Barroso JB (2017) Nitro-fatty acids in plant signaling: new key mediators of nitric oxide metabolism. Redox Biol 11:554–561PubMedPubMedCentralCrossRefGoogle Scholar
  125. Mata-Pérez C, Padilla MN, Sánchez-Calvo B, Begara-Morales JC, Valderrama R, Chaki M, Barroso JB (2018) Biological properties of nitro-fatty acids in plants. Nitric Oxide 78:176–179CrossRefGoogle Scholar
  126. McInnis SM, Desikan R, Hancock JT, Hiscock SJ (2006) Production of reactive oxygen species and reactive nitrogen species by angiosperm stigmas and pollen: potential signalling crosstalk? New Phytol 172:221–228PubMedCrossRefGoogle Scholar
  127. Men L, Wang Y (2007) The oxidation of yeast alcohol dehydrogenase-1 by hydrogen peroxide in vitro. J Proteome Res 6:216–225PubMedCrossRefGoogle Scholar
  128. Michelet L, Zaffagnini M, Vanacker H, Le Maréchal P, Marchand C, Schroda M, Lemaire SD, Decottignies P (2008) In vivo targets of S-thiolation in Chlamydomonas reinhardtii. J Biol Chem 283:21571–21578PubMedCrossRefGoogle Scholar
  129. Miller EW, Chang CJ (2007) Fluorescent probes for nitric oxide and hydrogen peroxide in cell signaling. Curr Opin Chem Biol 11:620–625PubMedPubMedCentralCrossRefGoogle Scholar
  130. Minas IS, Tanou G, Belghazi M, Job D, Manganaris GA, Molassiotis A, Vasilakakis M (2012) Physiological and proteomic approaches to address the active role of ozone in kiwifruit post-harvest ripening. J Exp Bot 63:2449–2464PubMedPubMedCentralCrossRefGoogle Scholar
  131. Molassiotis A, Fotopoulos V (2011) Oxidative and nitrosative signaling in plants: two branches in the same tree? Plant Signal Behav 6:210–214PubMedPubMedCentralCrossRefGoogle Scholar
  132. Mustafa AK, Gadalla MM, Sen N, Kim S, Mu W, Gazi SK, Barrow RK, Yang G, Wang R, Snyder SH (2009) H2S signals through protein S-Sulfhydration. Sci Signal 2:ra72PubMedPubMedCentralGoogle Scholar
  133. Nadtochiy SM, Burwell LS, Ingraham CA, Spencer CM, Friedman AE, Pinkert CA, Brookes PS (2009) In vivo cardioprotection by S-nitroso-2-mercaptopropionyl glycine. J Mol Cell Cardiol 46:960–968PubMedPubMedCentralCrossRefGoogle Scholar
  134. Nguyen AT, Donaldson RP (2005) Metal-catalyzed oxidation induces carbonylation of peroxisomal proteins and loss of enzymatic activities. Arch Biochem Biophys 439:25–31PubMedCrossRefGoogle Scholar
  135. Noctor G, Reichheld JP, Foyer CH (2017) ROS-related redox regulation and signaling in plants. Semin Cell Dev Biol 80:3–12PubMedCrossRefGoogle Scholar
  136. Nyström T (2005) Role of oxidative carbonylation in protein quality control and senescence. EMBO J 24:1311–1317PubMedPubMedCentralCrossRefGoogle Scholar
  137. Oracz K, Bouteau HEM, Farrant JM, Cooper K, Belghazi M, Job C, Job D, Corbineau F, Bailly C (2007) ROS production and protein oxidation as a novel mechanism for seed dormancy alleviation. Plant J 50:452–465PubMedCrossRefGoogle Scholar
  138. Padilla MN, Mata-Pérez C, Melguizo M, Barroso JB (2017) In vitro nitro-fatty acid release from Cys-NO2-fatty acid adducts under nitro-oxidative conditions. Nitric Oxide 68:14–22PubMedCrossRefGoogle Scholar
  139. Polge C, Jaquinod M, Holzer F, Bourguignon J, Walling L, Brouquisse R (2009) Evidence for the existence in Arabidopsis thaliana of the proteasome proteolytic pathway: activation in response to cadmium. J Biol Chem 284:35412–35424PubMedPubMedCentralCrossRefGoogle Scholar
  140. Prabakaran S, Lippens G, Steen H, Gunawardena J (2012) Post-translational modification: nature’s escape from genetic imprisonment and the basis for dynamic information encoding. Rev Syst Biol Med 4:565–583CrossRefGoogle Scholar
  141. Puyaubert J, Fares A, Rézé N, Peltier JB, Baudouin E (2014) Identification of endogenously S-nitrosylated proteins in Arabidopsis plantlets: effect of cold stress on cysteine nitrosylation level. Plant Sci 215–216:150–156PubMedCrossRefGoogle Scholar
  142. Queval G, Issakidis-Bourguet E, Hoeberichts FA, Vandorpe M, Gakière B, Vanacker H, Miginiac-Maslow M, Van Breusegem F, Noctor G (2007) Conditional oxidative stress responses in the Arabidopsis photorespiratory mutant cat2 demonstrate that redox state is a key modulator of daylength-dependent gene expression, and define photoperiod as a crucial factor in the regulation of H2O2-induced cell. Plant J 52:640–657PubMedCrossRefGoogle Scholar
  143. Radi RCNC (2004) Nitric oxide, oxidants, and protein tyrosine nitration. Proc Natl Acad Sci U S A 101:4003–4008PubMedPubMedCentralCrossRefGoogle Scholar
  144. Radi R (2013) Protein tyrosine nitration: biochemical mechanisms and structural basis of functional effects. Acc Chem Res 46:550–559PubMedCrossRefGoogle Scholar
  145. Rajjou L, Debeaujon I (2008) Seed longevity: survival and maintenance of high germination ability of dry seeds. C R Biol 331:796–805PubMedCrossRefGoogle Scholar
  146. Rajjou L, Lovigny Y, Groot SPC, Belghazi M, Job C, Job D (2008) Proteome-wide characterization of seed aging in Arabidopsis: a comparison between artificial and natural aging protocols. Plant Physiol 148:620–641PubMedPubMedCentralCrossRefGoogle Scholar
  147. Rajjou L, Duval M, Gallardo K, Catusse J, Bally J, Job C, Job D (2012) Seed germination and vigor. Annu Rev Plant Biol 63:507–533PubMedCrossRefGoogle Scholar
  148. Rao SR, Møller IM (2012) Pattern of occurrence and occupancy of carbonylation sites in proteins. J Proteome 11:4166–4173CrossRefGoogle Scholar
  149. Rey P, Bécuwe N, Barrault MB, Rumeau D, Havaux M, Biteau B, Toledano MB (2007) The Arabidopsis thaliana sulfiredoxin is a plastidic cysteine-sulfinic acid reductase involved in the photooxidative stress response. Plant J 49:505–514PubMedCrossRefGoogle Scholar
  150. Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot 53:103–110PubMedCrossRefPubMedCentralGoogle Scholar
  151. Romero-Puertas MC, Laxa M, Matte A, Zaninotto F, Finkemeier I, Jones AME, Perazzolli M, Vandelle E, Dietz KJ, Delledonne M (2007) S-Nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell Online 19:4120–4130CrossRefGoogle Scholar
  152. Romero-Puertas MC, Campostrini N, Mattè A, Righetti PG, Perazzolli M, Zolla L, Roepstorff P, Delledonne M (2008) Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response. J Proteome 8:1459–1469CrossRefGoogle Scholar
  153. Roos G, Foloppe N, Messens J (2013) Understanding the pK (a) of redox cysteines: the key role of hydrogen bonding. Antioxid Redox Signal 18:94–127PubMedCrossRefGoogle Scholar
  154. Rouhier N, Dos SCV, Tarrago L, Rey P (2006) Plant methionine sulfoxide reductase A and B multigenic families. Photosynth Res 89:247–262PubMedCrossRefPubMedCentralGoogle Scholar
  155. Rudolph V, Schopfer FJ, Khoo NKH, Rudolph TK, Cole MP, Woodcock SR, Bonacci G, Groeger AL, Golin-Bisello F, Chen CS, Baker PRS, Freeman BA (2009) Nitro-fatty acid metabolome: saturation, desaturation, β-oxidation, and protein adduction. J Biol Chem 284:1461–1473PubMedPubMedCentralCrossRefGoogle Scholar
  156. Rudolph V, Rudolph TK, Schopfer FJ, Bonacci G, Woodcock SR, Cole MP, Baker PRS, Ramani R, Freeman BA (2010) Endogenous generation and protective effects of nitro-fatty acids in a murine model of focal cardiac ischaemia and reperfusion. Cardiovasc Res 85:155–166PubMedCrossRefPubMedCentralGoogle Scholar
  157. Ruiz-May E, Segura-Cabrera A, Elizalde-Contreras JM, Shannon LM, Loyola-Vargas VM (2018) A recent advance in the intracellular and extracellular redox post-translational modification of proteins in plants. J Mol Recognit.  https://doi.org/10.1002/jmr.2754
  158. Rusterucci C, Espunya MC, Diaz M, Chabannes M, Martinez MC (2007) S-Nitrosoglutathione reductase affords protection against pathogens in Arabidopsis, both locally and systemically. Plant Physiol 143:1282–1292PubMedPubMedCentralCrossRefGoogle Scholar
  159. Ryšlavá H, Doubnerová V, Kavan D, Vaněk O (2013) Effect of posttranslational modifications on enzyme function and assembly. J Proteome 92:80–109CrossRefGoogle Scholar
  160. Saito S, Yamamoto-Katou A, Yoshioka H, Doke N, Kawakita K (2006) Peroxynitrite generation and tyrosine nitration in defense responses in tobacco BY-2 cells. Plant Cell Physiol 47:689–697PubMedCrossRefPubMedCentralGoogle Scholar
  161. Salmeen A, Andersen JN, Myers MP, Meng TC, Hinks JA, Tonks NK, Barford D (2003) Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 423:769–773PubMedCrossRefPubMedCentralGoogle Scholar
  162. Sánchez-Calvo B, Barroso JB, Corpas FJ (2013) Hypothesis: nitro-fatty acids play a role in plant metabolism. Plant Sci 199–200:1–6PubMedCrossRefPubMedCentralGoogle Scholar
  163. Sanz L, Albertos P, Mateos I, Sánchez-Vicente I, Lechón T, Fernández-Marcos M, Lorenzo O (2015) Nitric oxide (NO) and phytohormones crosstalk during early plant development. J Exp Bot 66:2857–2868PubMedCrossRefPubMedCentralGoogle Scholar
  164. Sawa T, Ihara H, Akaike T (2011) Antioxidant effect of a nitrated cyclic nucleotide functioning as an endogenous electrophile. Curr Top Med Chem 11:1854–1860PubMedCrossRefPubMedCentralGoogle Scholar
  165. Sawa T, Ihara H, Ida T, Fujii S, Nishida M, Akaike T (2013) Formation, signaling functions, and metabolisms of nitrated cyclic nucleotide. Nitric Oxide 34:10–18PubMedCrossRefGoogle Scholar
  166. Schopfer FJ, Baker PRS, Giles G, Chumley P, Batthyany C, Crawford J, Patel RP, Hogg N, Branchaud BP, Lancaster JR, Freeman BA (2005a) Fatty acid transduction of nitric oxide signaling: nitrolinoleic acid is a hydrophobically stabilized nitric oxide donor. J Biol Chem 280:19289–19297PubMedCrossRefGoogle Scholar
  167. Schopfer FJ, Lin Y, Baker PRS, Cui T, Garcia-Barrio M, Zhang J, Chen K, Chen YE, Freeman BA (2005b) Nitrolinoleic acid: an endogenous peroxisome proliferator-activated receptor ligand. Proc Natl Acad Sci U S A 102:2340–2345PubMedPubMedCentralCrossRefGoogle Scholar
  168. Schopfer FJ, Batthyany C, Baker PRS, Bonacci G, Cole MP, Rudolph V, Groeger AL, Rudolph TK, Nadtochiy S, Brookes PS, Freeman BA (2009) Detection and quantification of protein adduction by electrophilic fatty acids: mitochondrial generation of fatty acid nitroalkene derivatives. Free Radic Biol Med 46:1250–1259PubMedCrossRefGoogle Scholar
  169. Schopfer FJ, Cipollina C, Freeman BA (2011) Formation and signaling actions of electrophilic lipids. Chem Rev 111:5997–6021PubMedPubMedCentralCrossRefGoogle Scholar
  170. Sehrawat A, Abat JK, Deswal R (2013) RuBisCO depletion improved proteome coverage of cold responsive S-nitrosylated targets in Brassica juncea. Front Plant Sci 4:342PubMedPubMedCentralCrossRefGoogle Scholar
  171. Seth D, Stamler JS (2011) The SNO-proteome: causation and classifications. Curr Opin Chem Biol 15:129–136PubMedCrossRefPubMedCentralGoogle Scholar
  172. Shenton D, Grant CM (2003) Protein S-thiolation targets glycolysis and protein synthesis in response to oxidative stress in the yeast Saccharomyces cerevisiae. Biochem J 374:513–519PubMedPubMedCentralCrossRefGoogle Scholar
  173. Sies H (2017) Hydrogen peroxide as a central redox signaling molecule in physiological oxidative stress: oxidative eustress. Redox Biol 11:613–619PubMedPubMedCentralCrossRefGoogle Scholar
  174. Signorelli S, Corpas FJ, Borsani O, Barroso JB, Monza J (2013) Water stress induces a differential and spatially distributed nitro-oxidative stress response in roots and leaves of Lotus japonicus. Plant Sci 201–202:137–146PubMedCrossRefPubMedCentralGoogle Scholar
  175. Smakowska E, Czarna M, Janska H (2014) Mitochondrial ATP-dependent proteases in protection against accumulation of carbonylated proteins. Mitochondrion 19:245–251PubMedCrossRefPubMedCentralGoogle Scholar
  176. Song H, Fan P, Li Y (2009) Overexpression of organellar and cytosolic at HSP90 in arabidopsis thaliana impairs plant tolerance to oxidative stress. Plant Mol Biol Report 27:342–349CrossRefGoogle Scholar
  177. Souza JM, Peluffo G, Radi R (2008) Protein tyrosine nitration—functional alteration or just a biomarker? Free Radic Biol Med 45:357–366PubMedCrossRefGoogle Scholar
  178. Stadtman ER, Van Remmen H, Richardson A, Wehr NB, Levine RL (2005) Methionine oxidation and aging. Biochim Biophys Acta 1703:135–140PubMedCrossRefGoogle Scholar
  179. Sundaram S, Rathinasabapathi B (2010) Transgenic expression of fern Pteris vittata glutaredoxin PvGrx5 in Arabidopsis thaliana increases plant tolerance to high temperature stress and reduces oxidative damage to proteins. Planta 231:361–369PubMedCrossRefGoogle Scholar
  180. Tajc SG, Tolbert BS, Basavappa R, Miller BL (2004) Direct determination of thiol pK (a) by isothermal titration microcalorimetry. J Am Chem Soc 126:10508–10509PubMedCrossRefGoogle Scholar
  181. Takahashi M, Shigeto J, Sakamoto A, Izumi S, Asada K, Morikawa H (2015) Dual selective nitration in Arabidopsis: almost exclusive nitration of PsbO and PsbP, and highly susceptible nitration of four non-PSII proteins, including peroxiredoxin II E. Electrophoresis 36:2569–2578PubMedCrossRefGoogle Scholar
  182. Tamarit J (1998) Identification of the major oxidatively damaged proteins in Escherichia coli cells exposed to oxidative stress. J Biol Chem 273:3027–3032PubMedCrossRefGoogle Scholar
  183. Tanou G, Job C, Rajjou L, Arc E, Belghazi M, Diamantidis G, Molassiotis A, Job D (2009) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J 60:795–804PubMedCrossRefPubMedCentralGoogle Scholar
  184. Tanou G, Filippou P, Belghazi M, Job D, Diamantidis G, Fotopoulos V, Molassiotis A (2012) Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J 72:585–599PubMedCrossRefPubMedCentralGoogle Scholar
  185. Tarrago L, Laugier E, Zaffagnini M, Marchand C, Le Marechal P, Rouchier N, Lemaire SD, Rey P (2009) Regeneration mechanisms of Arabidopsis thaliana methionine sulfoxide reductases B by glutaredoxins and thioredoxins. J Biol Chem 284:18963–18971PubMedPubMedCentralCrossRefGoogle Scholar
  186. Tesnier K, Strookman-Donkers HM, van Pijlen JG, van der Geest AHM, Bino RJ, Groot SPC (2002) A controlled deterioration test for Arabidopsis thaliana reveals genetic variation in seed quality. Seed Sci Technol 30:149–165Google Scholar
  187. Trapet P, Kulik A, Lamotte O, Jeandroz S, Bourque S, Nicolas-Francès V, Rosnoblet C, Besson-Bard A, Wendehenne D (2015) NO signaling in plant immunity: a tale of messengers. Phytochemistry 112:72–79PubMedCrossRefGoogle Scholar
  188. Trostchansky A, Rubbo H (2008) Nitrated fatty acids: mechanisms of formation, chemical characterization, and biological properties. Free Radic Biol Med 44:1887–1896PubMedCrossRefGoogle Scholar
  189. Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Segal Floh EI, Scherer GFE (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47:346–354PubMedCrossRefPubMedCentralGoogle Scholar
  190. Turko IV (2002) Protein nitration in cardiovascular diseases. Pharmacol Rev 54:619–634PubMedCrossRefGoogle Scholar
  191. Valderrama R, Corpas FJ, Carreras A, Fernandez-Ocana A, Chaki M, Luque F, Gomez-Rodriguez MV, Colmenero-Varea P, del Rio LA, Barroso JB (2007) Nitrosative stress in plants. FEBS Lett 581:453–461PubMedCrossRefGoogle Scholar
  192. Vandenabeele S, Vanderauwera S, Vuylsteke M, Rombauts S, Langebartels C, Seidlitz HK, Zabeau M, Van Montagu M, Inzé D, Van Breusegem F (2004) Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. Plant J 39:45–58PubMedCrossRefGoogle Scholar
  193. Vandiver MS, Snyder SH (2012) Hydrogen sulfide: a gasotransmitter of clinical relevance. J Mol Med 90:255–263PubMedPubMedCentralCrossRefGoogle Scholar
  194. Vieira Dos Santos C, Cuiné S, Rouhier N, Rey P (2005) The Arabidopsis plastidic methionine sulfoxide reductase B proteins. Sequence and activity characteristics, comparison of the expression with plastidic methionine sulfoxide reductase A, and induction by photooxidative stress. Plant Physiol 138:909–922PubMedCrossRefGoogle Scholar
  195. Wang R (2012) Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev 92:791–896PubMedCrossRefGoogle Scholar
  196. Wang Y, Loake GJ, Chu C (2013) Cross-talk of nitric oxide and reactive oxygen species in plant programed cell death. Front Plant Sci 4:314PubMedPubMedCentralGoogle Scholar
  197. Waszczak C, Akter S, Jacques S, Huang J, Messens J, Van Breusegem F (2015) Oxidative post-translational modifications of cysteine residues in plant signal transduction. J Exp Bot 66:2923–2934PubMedCrossRefGoogle Scholar
  198. Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signalling in plants. Plant Cell Environ 31:622–631PubMedCrossRefGoogle Scholar
  199. Woo HA, Chae HZ, Hwang SC, Yang KS, Kang SW, Kim K, Rhee SG (2003) Reversing the inactivation of peroxiredoxins caused by cysteine sulfinic acid formation. Science 300:653–656PubMedCrossRefGoogle Scholar
  200. Wood ZA, Poole LB, Karplus PA (2003) Peroxiredoxin evolution and the signaling. Science 300:6506–6553CrossRefGoogle Scholar
  201. Xiong Y, Contento AL, Nguyen PQ, Bassham DC (2006) Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol 143:291–299PubMedCrossRefGoogle Scholar
  202. Yamasaki H, Sakihama Y, Takahashi S (1999) An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trend Plant Sci 4:128–129CrossRefGoogle Scholar
  203. Yang H, Mu J, Chen L, Feng J, Hu J, Li L, Zhou JM, Zuo J (2015) S -Nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiol 167:1604–1615PubMedPubMedCentralCrossRefGoogle Scholar
  204. Yoda H (2006) Polyamine oxidase is one of the key elements for oxidative burst to induce programmed cell death in tobacco cultured cells. Plant Physiol 142:193–206PubMedPubMedCentralCrossRefGoogle Scholar
  205. Yu M, Lamattina L, Spoel SH, Loake GJ (2014) Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytol 202:1142–1156PubMedCrossRefGoogle Scholar
  206. Yun BW, Feechan A, Yin M, Saidi NBB, Le Bihan T, Yu M, Moore JW, Kang JG, Kwon E, Spoel SH, Pallas JA, Loake GJ (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478:264–268PubMedCrossRefGoogle Scholar
  207. Zaffagnini M, Michelet L, Marchand C, Sparla F, Decottignies P, Le Maréchal P, Miginiac-Maslow M, Noctor G, Trost P, Lemaire SD (2007) The thioredoxin-independent isoform of chloroplastic glyceraldehyde-3- phosphate dehydrogenase is selectively regulated by glutathionylation. FEBS J 274:212–226PubMedCrossRefGoogle Scholar
  208. Zaffagnini M, Bedhomme M, Groni H, Marchand CH, Puppo C, Gontero B, Cassier-Chauvat C, Decottignies P, Lemaire SD (2012a) Glutathionylation in the photosynthetic model organism Chlamydomonas reinhardtii: a proteomic survey. Mol Cell Proteomics 11:M111.014142PubMedCrossRefGoogle Scholar
  209. Zaffagnini M, Bedhomme M, Marchand CH, Morisse S, Trost P, Lemaire SD (2012b) Redox regulation in photosynthetic organisms: focus on glutathionylation. Antioxid Redox Signal 16:567–586PubMedCrossRefGoogle Scholar
  210. Zaffagnini M, Morisse S, Bedhomme M, Marchand CH, Festa M, Rouhier N, Lemaire SD, Trost P (2013) Mechanisms of nitrosylation and denitrosylation of cytoplasmic glyceraldehyde-3-phosphate dehydrogenase from Arabidopsis thaliana. J Biol Chem 288:22777–22789PubMedPubMedCentralCrossRefGoogle Scholar
  211. Zafra A, Rodríguez-García MI, Alché JDD (2010) Cellular localization of ROS and NO in olive reproductive tissues during flower development. BMC Plant Biol 10:36PubMedPubMedCentralCrossRefGoogle Scholar
  212. Zagorchev L, Seal CE, Kranner I, Odjakova M (2013) A central role for thiols in plant tolerance to abiotic stress. Int J Mol Sci 14:7405–7432PubMedPubMedCentralCrossRefGoogle Scholar
  213. Zhang A, Zhang J, Zhang J, Ye N, Zhang H, Tan M, Jiang M (2011) Nitric oxide mediates brassinosteroid-induced ABA biosynthesis involved in oxidative stress tolerance in maize leaves. Plant Cell Physiol 52:181–192PubMedCrossRefGoogle Scholar
  214. Ziogas V, Tanou G, Filippou P, Diamantidis G, Vasilakakis M, Fotopoulos V, Molassiotis A (2013) Nitrosative responses in citrus plants exposed to six abiotic stress conditions. Plant Physiol Biochem 68:118–126PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • R. Valderrama
    • 1
  • J. C. Begara-Morales
    • 1
  • M. Chaki
    • 1
  • C. Mata-Pérez
    • 1
  • M. N. Padilla
    • 1
  • J. B. Barroso
    • 1
    Email author
  1. 1.Faculty of Experimental Sciences, Group of Biochemistry and Cell Signaling in Nitric Oxide, Department of Experimental Biology, Center for Advanced Studies in Olive Groves and Olive OilsUniversity of JaénJaénSpain

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