Peroxisomes sense and respond to environmental cues by regulating ROS and RNS signalling networks

Annals of Botany

Volumn 116, Issue 4, 2015, Pages 475-485

  Sandalio, L M ^a   Romero Puertas, M C ^a  

^a CSIC   (Spain)

Author keywords

Antioxidants; arabidopsis; autophagy; nitric oxide; nitrosative stress; oxidative stress; peroxisomes; photorespiration; reactive nitrogen species; reactive oxygen species; RNS; ROS; signalling; oxidation

Indexed keywords

ANTIOXIDANT; CELL ORGANELLE; DICOTYLEDON; ENVIRONMENTAL CUE; ENVIRONMENTAL STRESS; FATTY ACID; GENE EXPRESSION; HYDROGEN PEROXIDE; METABOLISM; NITRIC OXIDE; NITROGEN; OXIDATION; OXYGEN; PATHOGEN; PROTEIN; PROTEOMICS; REDOX CONDITIONS; RESPIRATION;

ARABIDOPSIS;

ANTIOXIDANT; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE;

METABOLISM; PEROXISOME; PLANT; SIGNAL TRANSDUCTION;

ANTIOXIDANTS; PEROXISOMES; PLANTS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84938913588     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcv074     Document Type: Review

References (114)

1. Antonenkov UD, Gronan S, Ohlmeier S, Hiltunen JK. (2010). Peroxisomes are oxidative organelles. Antioxidant Redox Signalling 13: 525-537
2. Baker A, Paudyal R. (2014). The life of the peroxisome: from birth to death. Current Opinion in Plant Biology 22: 39-47
3. Beligni MV, Fath A, Bethke PC, Lamattina L, Jones RL. (2002) Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiology 129: 1642-1650
4. Byrne RS, Hansche R, Mendel RR, Hille R. (2009). Oxidative half-reaction of arabidopsis thaliana sulfite oxidase: generation of superoxide by a peroxisomal enzyme. Journal of Biological Chemistry 284: 35479-35484
5. Cassin-Ross G, Hu J. (2014). Systematic phenotypic screen of arabidopsis peroxisomal mutants identifies proteins involved in b-oxidation. Plant Physiology 166: 1546-1559
6. Chaouch S, Queval G, Vanderauwera S, et al. (2010). Peroxisomal hydrogen peroxide is coupled to biotic defense responses by ISOCHORISMATE SYNTHASE1 in a daylength-related manner. Plant Physiology 153: 1692-1705
7. Chaouch S, Queval G, Vanderauwera S, et al. (2010). Peroxisomal hydrogen peroxide is coupled to biotic defense responses by ISOCHORISMATE SYNTHASE1 in a daylength-related manner. Plant Physiology 153: 1692-1705
8. Chaouch S, Queval G, Noctor G. (2012). AtRbohF is a crucial modulator of defence-associated metabolism and a key actor in the interplay between intracellular oxidative stress and pathogenesis responses in arabidopsis. Plant Journal 69: 613-627
9. Chen J, Vandelle E, Bellin D, Delledonne M. (2014). Detection and function of nitric oxide during the hypersensitive response in arabidopsis thaliana: where theres a will theres a way. Nitric Oxide 43: 81-88
10. Corpas FJ, Barroso JB. (2014). Peroxisomal plant nitric oxide synthase (NOS) protein is imported by peroxisomal targeting signal type 2 (PTS2) in a process that depends on the cytosolic receptor PEX7 and calmodulin. FEBS Letters 588: 2049-2054
11. 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 Physiology 121: 921-928
12. Corpas FJ, Barroso JB, Carreras A, et al. (2004). Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiology 136: 2722-2733
13. Corpas FJ, Hayashi M, Mano S, Nishimura M, Barroso JB. (2009). Peroxisomes are required for in vivo nitric oxide accumulation in the cytosol following salinity stress of arabidopsis plants. Plant Physiology 151: 2083-2094
14. Corpas FJ, Leterrier M, Begara-Morales JC, et al. (2013). Inhibition of peroxisomal hydroxypyruvate reductase (HPR1) by tyrosine nitration. Biochimica et Biophysica Acta 1830: 4981-4989
15. Costa A, Drago IO, Behera S, et al. (2010). H2O2 in plant peroxisomes: an in vivo analysis uncovers a Ca2-dependent scavenging system. Plant Journal 62: 760-772
16. Dietz KJ. (2003). Plant peroxiredoxins. Annual Review of Plant Biology 54: 93-107
17. Distefano S, Palma JM, McCarthy I, del Río LA. (1999). Proteolytic cleavage of plant proteins by peroxisomal endoproteases from senescent pea leaves. Planta 209: 308-313
18. Dixon DP, Hawkins T, Hussey PJ, Edwards R. (2009). Enzymes activities and subcellular localization of members of the arabidopsis glutathione transferase superfamily. Journal of Experimental Botany 60: 1207-1218
19. Droillard MJ, Paulin A. (1990). Isozymes of superoxide dismutase in mitochondria and peroxisomes isolated from petals of carnation (Dianthus caryophyllus) during senescence. Plant Physiology 94: 1187-1192
20. Du H, Kim S, Nam KH, et al. (2010). Identification of uricase as a potential target of plant thioredoxin: implication in the regulation of nodule development. Biochemical and Biophysical Research Communications 18: 22-26
21. Farmer LM, Rinaldi MA, Young PG, Danan CH, Burkhart SE, Bartel B. (2013). Disrupting autophagy restores peroxisome function to an arabidopsis lon2 mutant and reveals a role for the LON2 protease in peroxisomal matrix protein degradation. Plant Cell 25: 4085-4100
22. Foyer CH, Noctor G. (2003). Redox sensing and signalling associated with reactive oxygen species in chloroplasts, peroxisomes and mitochondria. Physiologia Plantarum 119: 355-364
23. Foyer CH, Noctor G. (2011). Ascorbate and glutathione: the heart of the redox hub. Plant Physiology 155: 2-18
24. Foyer CH, Bloom AJ, Queval G, Noctor G. (2010). Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annual Review of Plant Biology 60: 455-484
25. Gechev TS, Minkov IN, Hille J. (2005). Hydrogen peroxide induced cell death in arabidopsis: transcriptional and mutant analysis reveals a role of an oxoglutarate-dependent dioxygenase gene in the cell death process. International Union of Biochemistry and Molecular Biology Life 57: 181-188
26. Godber ELJ, Doel JJ, Sapkota PG, et al. (2000). Reduction of nitrite to nitric oxide catalysed by xanthine oxidoreductase. Journal of Biological Chemistry 275: 7757-7763
27. Goyer A, Johnson TL, Olsen LJ, et al. (2004). Characterization and metabolic function of a peroxisomal sarcosine and pipecolate oxidase from arabidopsis. Journal of Biological Chemistry 279: 16947-16953
28. Gupta KJ, Fernie AR, Kaiser WM, van Dongen JT. (2011). On the origins of nitric oxide. Trends in Plant Science 16: 160-168
29. Hackenberg T, Juul T, Auzina A, et al. (2013). Catalase and NO CATALASE ACTIVITY1 promote autophagy-dependent cell death in arabidopsis. Plant Cell 25: 4616-4626
30. Halliwell B, Gutteridge JMC. (2007). Free radicals in biology and medicine. Oxford: Oxford University Press
31. Hölscher C, Meyer T, von Schaewen A. (2014). Dual-targeting of arabidopsis 6-phosphogluconolactonase 3 (PGL3) to chloroplasts and peroxisomes involves interaction with Trxm2 in the cytosol. Molecular Plant 7: 252-255
32. Hooks MA (2002). Molecular biology, enzymology, and physiology of b-oxidation. In: A Baker, IA Graham. eds. Plant peroxisomes. London: Kluwer Academic Publishers, 19-55
33. Hu J, Baker A, Bartel B, et al. (2012). Plant peroxisomes: biogenesis and function. Plant Cell 24: 2279-2303
34. Huang AHC, Trelease RN, Moore TS Jr. (1983). Plant peroxisomes. New York: Academic Press
35. Inzé A, Vanderauwera S, Hoeberichts FA, Vandorpe M, Van Gaever T, Van Breusegem F. (2012). A subcellular localization compendium of hydrogen peroxide-induced proteins. Plant, Cell and Environment 35: 308-320
36. 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 Physiology 114: 275-284
37. Kamada-Nobusada T, Hayashi M, Fukazawa M, Sakakibara H, Nishimura M. (2008). A putative peroxisomal polyamine oxidase, AtPAO4, is involved in polyamine catabolism in arabidopsis thaliana. Plant and Cell Physiology 49: 1272-1282
38. Kataya ARA, Reumann S. (2010). Arabidopsis glutathione reductase 1 is dually targeted to peroxisomes and the cytosol. Plant Signaling and Behavior 5: 171-175
39. Kaur N, Reumann S, Hu J. (2009). Peroxisome biogenesis and function. In: The arabidopsis book 7: e0123. doi: 10.1199/tab.0123
40. Kerchev P, Mühlenbock P, Denecker J, et al. (2015). Activation of auxin signalling counteracts photorespiratory H2O2-dependent cell death. Plant, Cell and Environment 38: 253-265
41. Koh S, Andre A, Edwards H, Ehrhardt D, Somerville S. (2005). Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. Plant Journal 44: 516-529
42. Kumar S, Kawałek A, Van Der Klei IJ. (2014). Peroxisomal quality control mechanisms. Current Opinion in Microbiology 22: 30-37
43. Kuzniak E, Skłodowska M. (2005). Fungal pathogen-induced changes in the antioxidant systems of leaf peroxisomes from infected tomato plants. Planta 222: 192-200
44. Laspina NV, Groppa MD, Tomaro ML, Benavides MP. (2005). Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Science 169: 323-330
45. 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 Physiology 138: 2111-2123
46. Li S, Mhamdi A, Trotta A, Kangasjärvi S, Noctor G. (2014). The protein phosphatase subunit PP2A-B0c is required to suppress day length-dependent pathogenesis responses triggered by intracellular oxidative stress. New Phytologist 202: 145-160
47. Linka N, Theodoulou FL. (2013). Metabolite transporters of the plant peroxisomal membrane: known and unknown. Sub-cellular Biochemistry 69: 169-194
48. Lisenbee CS, Heinze M, Trelease RN. (2003). Peroxisomal ascorbate peroxidase resides within a subdomain of rough endoplasmic reticulum in wild-type arabidopsis cells. Plant Physiology 132: 870-882
49. Lisenbee CS, Lingard MJ, Trelease RN. (2005). Arabidopsis peroxisomes possess functionally redundant membrane and matrix isoforms of monodehydroascorbate reductase. Plant Journal 43: 900-914
50. López-Huertas E, Charlton WL, Johnson B, Graham IA, Baker A. (2000). Stress induces peroxisome biogenesis genes. EMBO Journal 19: 6770-6777
51. Lozano-Juste J, Colom-Moreno R, León J. (2011). In vivo protein tyrosine nitration in arabidopsis thaliana. Journal of Experimental Botany 62: 3501-3017
52. Ma C, Hagstrom D, Polley SG, Subramani S. (2013). Redox-regulated cargo binding and release by the peroxiosomal targeting signal receptor, Pex5. Journal of Biological Chemistry 288: 27220-27231
53. Mano J, Nagata M, Okamura S, Shiraya T, Mitsui T. (2014). Identification of oxidatively modified proteins in salt-stressed arabidopsis: a carbonyl-targeted proteomics approach. Plant and Cell Physiology 55: 1233-1244
54. Mhamdi A, Noctor G. (2015). Analysis of the roles of the arabidopsis peroxisomal isocitrate dehydrogenase in leaf metabolism and oxidative stress. Environmental and Experimental Botany 114: 22-29
55. Mhamdi A, Hager J, Chaouch S, et al. (2010). Arabidopsis GLUTATHIONE REDUCTASE1 plays a crucial role in leaf responses to intracellular hydrogen peroxide and in ensuring appropriate gene expression through both salicylic acid and jasmonic acid signaling pathways. Plant Physiology 153: 1144-1160
56. Mhamdi A, Noctor G, Baker A. (2012). Plant catalases: peroxisomal redox guardians. Archives of Biochemistry and Biophysics 525: 181-194
57. De Michele R, Vurro E, Rigo C, et al. (2009). Nitric oxide is involved in cadmium-induced programmed cell death in arabidopsis suspension cultures. Plant Physiology 150: 217-228
58. Mittler R, Vanderauwera S, Suzuki N, et al. (2011). ROS signaling: the new wave?. Trends in Plant Science 16: 300-309
59. McCarthy-Suárez I, Gómez M, del Río LA, Palma JM. (2011). Role of peroxisomes in the oxidative injury induced by the auxin herbicide 2, 4-D in leaves of pea plants. Biologia Plantarum 55: 485-492
60. Mitsuya S, El Shami M, Sparkes IA, et al. (2011). Salt stress causes peroxisome proliferation, but inducing peroxisome proliferation does not improve NaCl tolerance in arabidopsis thaliana. PLoS One 5: e9408
61. Møller IM, Sweetlove LJ. (2010). ROS signalling-specificity is required. Trends in Plant Science 15: 370-374
62. Mor A, Koh E, Weiner L, Rosenwasser S, Sibony-Benyamini H, Fluhr R. (2014). Singlet oxygen signatures are detected independent of light or chloroplasts in response tomultiple stresses. Plant Physiology 165: 249-261
63. Moreau M, Lindermayr C, Durner J, Klessig DK. (2010). NO synthesis and signaling in plants -where do we stand?. Physiologia Plantarum 138: 372-383
64. Mur LAJ, Hebelstrup KH, Gupta KJ. (2013). Striking a balance: does nitrate uptake and metabolism regulate both NO generation and scavenging?. Frontiers in Plant Science 4: 288
65. Murakami K, Ichinohe Y, Koike M. (2013). VCP is an integral component of a novel feedback mechanism that controls intracellular localization of catalase and H2O2 levels. PLoS One 8: e56012
66. Neill S, Bright J, Desikan R, Hancock J, Harrison J, Wilson I. (2008). Nitric oxide evolution and perception. Journal of Experimental Botany 59: 25-35
67. Noctor G, Queval G, Mhamdi A, Chaouch S, Foyer C. (2011). Glutathione. The arabidopsis book 9: 1-32. doi: 10.1199/tab.0142
68. Nguyen AT, Donaldson RP. (2005). Metal-catalyzed oxidation induces carbonylation of peroxisomal proteins and loss of enzymatic activities. Archives in Biochemistry and Biophysics 439: 25-31
69. Nordgren M, Fransen M. (2014). Peroxisomal metabolism and oxidative stress. Biochimie 98: 56-62
70. Oksanen E, Haikio E, Sober J, Karnosky DF. (2003). Ozone-induced H2O2 accumulation in field-grown aspen and birch is linked to foliar ultrastructure and peroxisomal activity. New Phytologist 161: 791-799
71. Ortega-Galisteo AP, Rodríguez-Serrano M, Pazmiño DM, Gupta DK, Sandalio LM, Romero-Puertas MC. (2012). S-Nitrosylated proteins in pea (Pisum sativum L) leaf peroxisomes: changes under abiotic stress. Journal of Experimental Botany 63: 2089-2103
72. Osno Y, Kim DW, Watanabe K, et al. (2012). Constitutively and highly expressed Oryza sativa polyamine oxidases localize in peroxisomes and catalyze polyamine back conversion. Amino Acids 42: 867-876
73. Pacher P, Beckman JS, Liaudet L (2007). Nitric oxide and peroxynitrite in health and disease. Physiological Review 87: 315-424
74. Pazmiño MD, Rodríguez-Serrano M, Sanz M, Romero-Puertas MC, Sandalio LM. (2014). Regulation of epinasty induced by 2, 4-dichlorophenoxyacetic acid in pea and arabidopsis plants. Plant Biology 16: 809-818
75. Planas-Portell J, Gallart M, Tiburcio AF, Altabella T. (2013). Coppercontaining amine oxidases contribute to terminal polyamine oxidation in peroxisomes and apoplast of arabidopsis thaliana. BMC Plant Biology 13: 109
76. Prado AM, Porterfield DM, Feijó JA. (2008). Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 131: 2707-2714
77. Quan S, Yang P, Cassin-Ross G, et al. (2013). Proteome analysis of peroxisomes from etiolated arabidopsis seedlings identifies a peroxisomal protease involved in beta-oxidation and development. Plant Physiology 163: 1518-1538
78. Queval G, Issakidis-Bourguet E, Hoeberichts FA, et al. (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 death. Plant Journal 52: 640-657
79. Queval G, Neukermans J, Vanderauwera S, Van Breusegem F, Noctor G. (2012). Day length is a key regulator of transcriptomic responses to both CO2 and H2O2 in arabidopsis. Plant, Cell and Environment 35: 374-387
80. Reumann S, Quan S, Aung K, et al. (2009). In-depth proteome analysis of arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes. Plant Physiology 150: 125-143
81. del Río LA. (2011). Peroxisomes as a cellular source of reactive nitrogen species signal molecules. Archives of Biochemistry and Biophysics 506: 1-11
82. del Río LA, Pastori GM, Palma JM, et al. (1998). The activated oxygen role of peroxisomes in senescence. Plant Physiology 116: 1195-1200
83. Rizhsky L, Hallak-Herr E, Van Breusegem F, et al. (2002). Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant Journal 32: 329-342
84. Rodríguez-Serrano M, Romero-Puertas MC, Pastori GM, et al. (2007). Peroxisomal membrane manganese superoxide dismutase: characterization of the isozyme from watermelon. Journal of Experimental Botany 58: 2417-2427
85. Rodríguez-Serrano M, Romero-Puertas MC, Sparkes I, Hawes C, del Río LA, Sandalio LM. (2009). Peroxisome dynamics in arabidopsis plants under oxidative stress induced by cadmium. Free Radicals in Biology and Medicine 47: 1632-1639
86. Rodríguez-Serrano M, Pazmiño DM, Sparkes I, et al. (2014). 2, 4-Dichlorophenoxyacetic acid promotes S-nitrosylation and oxidation of actin affecting cytoskeleton and peroxisomal Dynamics. Journal of Experimental Botany 65: 4783-4793
87. Rojas CM, Senthil-Kumar M, Wang K, Ryu C-M, Kaundal A, Mysore K. (2012). Glycolate oxidase modulates reactive oxygen species-mediated signal transduction during no host resistance in Nicotiana benthamiana and Arabidopsis. Plant Cell 24: 336-352
88. Romero-Puertas MC, Palma JM, Gómez M, del Río LA, Sandalio LM. (2002). Cadmium causes the oxidative modification of proteins in pea plants. Plant, Cell and Environment 25: 677-686
89. Romero-Puertas MC, Rodríguez Serrano M, Corpas FJ, Gómez M, del Río LA, Sandalio LM. (2004). Cadmium-induced subcellular accumulation of O2-and H2O2 in pea leaves. Plant, Cell and Environment 27: 1122-1134
90. Romero-Puertas MC, Corpas FJ, Sandalio LMet al. (2006). Glutathione reductase from pea leaves: response to abiotic stress and characterization of the peroxisomal isozyme. New Phytologist 170: 43-52
91. Rosenwasser S, Rot I, Sollner E, et al. (2011). Organelles contribute differentially to reactive oxygen species-related events during extended darkness. Plant Physiology 156: 185-201
92. Sandalio LM, Fernández VM, Rupérez FL, del Río LA. (1988). Superoxide free radicals are produced in glyoxysomes. Plant Physiology 87: 1-4
93. Sandalio LM, Rodríguez-Serrano M, Romero-Puertas MC, del Río LA. (2013). Role of peroxisomes as a source of reactive oxygen species (ROS) signaling molecules. Sub-cellular Biochemistry 69: 231-255
94. Schlicht M, Ludwig-Müller J, Burbach C, Volkmann D, Baluska F. (2013). Indole-3-butyric acid induces lateral root formation via peroxisome-derived indole-3-acetic acid and nitric oxide. New Phytologist 200: 473-482
95. Sewelam N, Jasperta N, Van Der Kelenc K, et al. (2014). Spatial H2O2 signaling specificity: H2O2 from chloroplasts and peroxisomes modulates the plant transcriptome differentially. Molecular Plant 7: 1191-1210
96. Shibata M, Oikawa K, Yoshimoto K, et al. (2013). Highly oxidized peroxisomes are selectively degraded via autophagy in arabidopsis. Plant Cell 25: 4967-4983
97. Shibata M, Oikawa K, Yoshimoto K, et al. (2014). Plant autophagy is responsible for peroxisomal transition and plays an important role in the maintenance of peroxisomal quality. Autophagy 10: 936-937
98. Sinclair AM, Trobacher CP, Mathur N, Greenwood JS, Mathur J. (2009). Peroxule extension over ER-defined paths constitutes a rapid subcellular response to hydroxyl stress. Plant Journal 59: 231-242
99. Stolz DB, Zamora R, Vodovotz Y. (2002). Peroxisomal localization of inducible nitric oxide synthase in hepatocytes. Hepatology 36: 81-93
100. Stuehr D, Pou S, Rosen GM. (2001). Oxygen reduction by nitric oxide synthases. Journal of Biological Chemistry 276: 14533-14536
101. Suzuki N, Koussevitzky S, Mittler R, Miller G. (2012). ROS and redox signalling in the response of plants to abiotic stress. Plant, Cell and Environment 35: 259-270
102. Takahashi H, Chen Z, Du H, Liu Y, Klessig DF. (1997). Development of necrosis and activation of disease resistance in transgenic tobacco plants with severely reduced catalase levels. Plant Journal 11: 993-1005
103. Taler D, Galperin M, Benjamion I, Cohen Y, Kenigsbuch D. (2004). Plant eR genes that encode photorespiratory enzymes confer resistance against disease. Plant Cell 16: 172-184
104. Tognetti VB, Mühlenbock P, Van Breusegem F. (2012). Stress homeostasis -the redox and auxin perspective. Plant, Cell and Environment 35: 321-333
105. Valenzuela-Soto JH, Iruegas-Bocardo F, Martínez-Gallardo NA, Molina-Torres J, Gómez-Lim MA, Délano-Frier JP. (2011). Transformed tobacco (Nicotiana tabacum) plants over-expressing a peroxisome proliferator-activated receptor gene from Xenopus laevis (xPPARa) show increased susceptibility to infection by virulent Pseudomonas syringae pathogens. Planta 233: 507-521
106. Vanaker H, Sandalio LM, Jiménez A, et al. (2006). Roles for redox regulation in leaf senescence of pea plants grown on different sources of nitrogen nutrition. Journal of Experimental Botany 57: 1735-1746
107. Vandenabeele S, Vanderauwera S, Vuylsteke M, et al. (2004). Catalase deficiency drastically affects gene expression induced by high light in arabidopsis thaliana. Plant Journal 39: 45-58
108. Vanderauwera S, Zimmermann P, Rombauts S, et al. (2005). Genome-wide analysis of hydrogen peroxide-regulated gene expression in arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiology 139: 806-821
109. Vanderauwera S, Suzuki N, Miller G, et al. (2011). Extranuclear protection of chromosomal DNA from oxidative stress. Proceedings of the National Academy of Sciences of the USA 108: 1711-1716
110. Verdoucq L, Vignols F, Jacquot JP, Chartier Y, Meyer Y. (1999). In vivo characterization of a thioredoxin h target protein defines a new peroxiredoxin family. Journal of Biological Chemistry 274: 19714-19722
111. Waller JC, Dhanoa PK, Schumann U, Mullen RT, Snedden WA. (2010). Subcellular and tissue localization of NAD kinases from arabidopsis: compartmentalization of De novo NADP biosynthesis. Planta 231: 305-317
112. Wimalasekera R, Tebartz F, Scherer GH. (2011). Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Science 181: 593-603
113. Yin H, Xu L, Porter NA. (2011). Free radical lipid peroxidation: mechanism and analysis. Chemical Reviews 111: 5944-5972
114. Yun B-W, Spoel SH, Loake GJ. (2012). Synthesis of and signalling by small, redox active molecules in the plant immune response. Biochimica et Biophysica Acta 1820: 770-776